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ILLINOIS BIOLOGICAL 
MONOGRAPHS 


PUBLISHED QUARTERLY 
UNDER THE AUSPICES OF THE GRADUATE SCHOOL 
BY THE UNIVERSITY OF ILLINOIS 


VOLUME xX 


Urbana, Illinois 


1926 


EpItoRIAL COMMITTEE 


STEPHEN ALFRED FORBES WILLIAM TRELEASE 


HENRY BALDWIN WARD 


TABLE OF CONTENTS 


VOLUME X 


NUMBERS 


1. Studies on the Avian Species of the Cestode Family Hymenolepididae. 
7 By R. L. Mayhew. With 9 plates and 2 text figures. . 


2. Some North American Fish Trematodes. By H. W. Manter. With 6 
plates, 2 charts, and 1 text figure 


3. Comparative Studies on Furcocercous Cercariae. By H. M. Miller, Jr. 
With 8 plates and 2 text figures ; 


4. A Comparison of the Animal Communities of Coniferous and Deciduous 
Forests. By I. H. Blake, With 16 plates and 25 tables 


1-126 


127-264 


265-370 


371-520 


Digitized by the Internet Archive 
in 2011 with funding from 
University of Illinois Urbana-Champaign 


http://www.archive.org/details/somenorthamerical1Omant 


SOME NORTH AMERICAN FISH 
TREMATODES 


WITH 6 PLATES, 2 CHARTS AND 1 TEXTFIGURE 


BY 


HAROLD WINFRED MANTER 


Contributions from the 
ee Laboratory of the paiveraty of inate 
under the direction ot Henry B. War 


THESIS 


SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE 
DEGREE OF DOCTOR OF PHILOSOPHY IN ZOOLOGY IN THE GRADUATE 
SCHOOL OF THE UNIVERSITY OF ILLINOIS 


1925 


TABLE OF CONTENTS 


Introduction. . ssibdetiayd divas egsile) Poe aith dha ateustiite Suseta shane aye e-ce enero te, Pea db aie rele oes 
Material and Methods...........0.cccceccceccceeeucceecccsecceeunee. 
General Distribution of Entozoa in Hosts Examined. 
Historical Survey. . Ses caren einai ets 
The Morphology of Otodistomum cestoides. Edi diGuveeoentsgalscamenecev ens ee 
Thickness of Regions of Body Wall. . Tae srae Pata Roses cite ae ernie maton 
Qbodastoragn Vela POT stata see: sce:0e scares scuah oa auhy sks daemon edooaisl dual dibntcbavaiquyace avace.ik,@las aces 
Olods stom COSLOTE ESS os c.508 wae im seo 0ie,a(s wae o 6 Reise wv edie 6 Ale 6 ee DeLee Oe cee 
Variation in Posterior Extent of Vitellaria in O. cestoides. . Deviate oe emia 
Growth Changes in Otodistomum cestoides Within the Final Host..............--- 
Chart I—Showing Relations Between Body Length and Distance from the 
Anterior End to Ventral Sucker in O. cesfoides.... 2... cece eee ee eee 


COLD ES sitar orcs cia Gisinrs Soloists S visleeiaie aie oisicss\pibie Sins Bore, SF eae ae wie eres 


Comparison of Uterus Region with Posterior Body Region in Young Specimens 
Of Olodistonttii CeStOId eS <5 oc ee signe 6 dae es sos Cease os e805 8b ee88 
Comparison of Uterus Region with Posterior Body Region in Adult Specimen 
OL OL0dtSLOMITA.COSLOMLOS = = sina, dioreiess diatazs seis 6: cers iol evaveie- tis skelecn.esiaiete e838 
Comparison of Neck Region with Posterior Body Region in Young Specimens 
OL OLOdtSLO DUMMY COSLOUDES oo. oxc: ect nseserereleie ciate as Wio16s0 8 46 oe a taleCorosecs & 
Comparison of Neck Region with Posterior Body Region in Adult Specimens 
Of Ofodistomune Cestoides... o.oo ccicneessceccteeticee tse ssvectoe 
Diagram to Show Growth Changes in Otodistomum cestoides................ 
Comparison of Ofodistomum cestoides and O. veli, eure Rae eater a alate mete nee ares e 
The Miracidium of Otodistomum cestoides. . ee 
Notes on the Life History of Otodistomum cestoides.. 
A Systematic Review of the Family Azygiidae. . Pe thatele tas teenth Ca Gvee renee Sas 
Azygia angusticauda (Stafford ron bial gia Sr atesa sav hier 4 ol ieee a wresdsl cera ee Redvers Scene 
Azygia acuminata Goldberger 1911. . si gvtiaee ar eirolaus's ovaliera see e-ayGiai dis Guanes 
Azygialonga (Leidy 1851)....... e aay bare rtsus helena oc Meu taaeeta reer a cue afhcith cuemeea 
ASV OIG SEDELO sooo swresss.noe tinea oes Op etle Gale Hale emee eS Ee bent 
ALLY BUD DULOOSE aici uatate le wiviviche oa1s'cixiereidiel orale sie latelare atens ansie aradaig year 
Cooper’s Asygialuciit from L. Ronen) eRe Si oie Mee ea tet ear ete 
pecber) Tee in fom peaks Beant atataeknic’s ae oN os wien ors 
Azygia robusta Odhner 1911. vette 
Azygia perryii Fujita 1918. . Monet ee eree ye Mee area cne 
Azygia volgensis (v. Linstow) Odhner 1911............... 0.2. s seers ee eee 
Synopsis of the Genus Azygia. . ficeiate eyclerd Aiaas os Merieete ets 
A General Study of Some Marine Fish Trematodes. . Sa, Micke ius, Sue. daria eared 
The: Genus Podocotyles acc vsa0 os te cecds mecca Sicha ee neue been sade ete 
Podocotyle atomon (Rudolphi 1802)... 2.2... 06. 
Podocotyle olssoni Odhner 1905..... 
Stephaochasmus baccatus Nicoll 1907. . 
Lepidapedon rachion (Cobbold) Stafford 1904. 
Lepidapedon elongatum (Lebour 1908)... eerie eerie emer es 
Homalometron pallidum Stafford 1904... 00006 cece eee 
Steganoderma formosum Stafford 1904.2... 600 e eee eee 
MhePlemiuridaes.:.,. o.siecsisavareeai sities @ sie. snes aun eee Dede ee meee 
Hemiuris levinsent Odbner 1905.20... oc. cs cece nn cseeeecea ceaetacesese 
Brachylhallus crenatus (Rudolphi 1802)... 2. 0.0.6 eee 
Lecithaster gibbosus (Rudolphi 1802).......000 00 0c cee eee eee 
A ponurus sphaerolecithus Manter 1925........000 00 eee ee eee 
Genolinea laticauda Manter 1925. ...ic.06 2 ccs oe cee tones tesa beens s 
Gonocerca phycidis Manter 1925......... 2.000. - cece cece ect e ee en tenes 
Derogenes varicus (Miiller 1784).....0 00000 ec ce eee e eens 
Hirudinella fusca (Poirier 1885). . etapa shvavanese) Hier aera srearary aero ete 
Siphodera vinaledwardsii (Linton 1899). jase ifindutautaalanpetneenirees.e 
Deropristis inflata (Molin 1859)... 2.2.0. cece eee ee nee ence nen eeeeens 
Acanthocotyle verrilli Goto 1899... cece eet e en eee 
Dactylocotyle minor (Olsson 1868)... . Reet are ene Saran 
Summary and Conclusions.... 2.0... 0606 ce ence cece teen aces 
Bibliography. . eee 
Explanation of Plates. . 
Index to Scientific Names. . 


133] SOME NORTH AMERICAN FISH TREMATODES—MANTER 7 


INTRODUCTION 


The study of the parasites of North American fish, especially marine 
species, offers a comparatively new field to the investigator. Linton has 
opened this field in a broad sense by his papers on fish parasites of the 
Woods Hole region and of the Atlantic waters of Southern United States, 
This pioneer work has been necessarily incomplete in some respects. On 
the parasites of fishes inhabiting the colder waters of the northern Atlantic, 
almost no work has been done in America. Stafford and Cooper have made 
small collections in these regions. On European shores considerably more 
research has been done, and here the early work of Van Beneden, Olsson, 
and Levinsen has been followed by valuable contributions from Looss, 
Odhner, Lebour, Nicoll, and others. 

The present paper is based very largely upon studies of marine fish 
parasites from the Maine coast. These studies were first undertaken at 
the Mount Desert Island Biological Laboratory during the summer of 
1924, although some material was also collected in the same region in 1923, 
Early in the work of collection, attention was directed to a common 
trematode (Ofodistomum cestoides) of the barn-door skate. Considerable 
time was devoted to the structure of this form and its life history. Later, 
a large series of fresh-water forms related to this species were also studied 
and compared. A brief report of the trematodes collected from marine 
fish has already been published (Manter, 1925). 

Sincere appreciation is here extended to Professor Ulric Dahlgren for 
the use of the laboratory facilities at the Mount Desert Island Biological 
Station. Acknowledgment is also rendered to the Hygienic Laboratory of 
the U. S. Public Health Service and to the U. S. National Museum for the 
loan of valuable material. Above all, is the writer indebted to Dr. Henry B. 
Ward, under whose direction these studies were undertaken. To him 
appreciation is extended, not only for his constant interest, but also for 
the loan of material from his personal collection of parasites, and for the 
use of his extensive library. To others, who, like fellow-students, have been 
less intimately associated with this work, but who have gladly cooperated 
in many ways, gratitude is likewise expressed. 


MATERIAL AND METHODS 


The collection of parasites was not limited to any particular group. 
In general, a broad collection of metazoan fish parasites was attempted. 
The final collection included trematodes, cestodes, nematodes, acantho- 


8 ILLINOIS BIOLOGICAL MONOGRAPHS (134 


cephala, copepods, leeches, an ectoparasitic turbellarian, and an ecto- 
parasitic isopod. From this collection the trematodes were chosen for 
special study. 

The most common shore fish such as sculpin, flounder, herring, and 
skates were obtained from Frenchman’s Bay in the immediate vicinity of 
the Laboratory. Most of the fish examined, however, were obtained at the 
small fishing village of Manset on the south side of Mount Desert Island. 
Here specimens of the larger food fish such as cod, haddock, and hake were 
available in large numbers. Identification of the host was usually simple as 
most of the fish examined were common and well known species. Some 
uncertainty was unavoidable in the correct identification of a few forms, 
such as the sculpins. 


The following table (Table 1) shows the general occurrence of the 
different groups of parasites according to hosts. 


TABLE 1 
GENERAL DISTRIBUTION OF ENTOZOA IN Hosts EXAMINED 


Name of Host Number of Hosts 


With With 


ee With With 
Scientific Common Examined | Trema- | Nema- Ces- | Acantho- 
. todes todes todes | cephala 
Acanthias vulgaris | Common dog 
fish 12 2 12 
Raia erinacea Bonnet skate 8 1 1 8 
Raia diaphanes Big skate 2 2 1 
Raia stabuliforis Barn-door skate 20 18 7 20 
Raia scabrata (?) Skate 1 1 1 
Anguilla chrysypa | Common eel 2 2 
Clupea harengus Herring 28 9 6 
Osmerus mordax Smelt 5 3 2 
Scomberscombrus | Mackerel 5 5 
Fundulus Killifish, 
heteroclitus minnow 25 9 6 23 
Tautogolabrus 
adspersus Cunner 4 3 1 


135] SOME NORTH AMERICAN FISH TREMATODES—MANTER 9 


TaBLe 1 (continued) 


Name of Host Number of Hosts 


ee With With With With 
Scientific Common Examined | Trema- | Nema- Ces- |Acantho- 
todes todes todes cephala 


Myxocephalus 

octodecimspinosus | Sculpin 11 3 7 4 9 
Pholis gunnellus Butterfish 9 w 

Anarrhichaslupus | Wolf-fish 2 1 1 

Zoarces anguillaris | Eel pout 1 1 
Pollachius virens Pollack 4 2 3 2 
Gadus callarias Cod 10 8 9 2 10 
Melanogrammus 

aeglifinus Haddock 17 4 9 5 17 
Urophycis tenuis Hake 3 3 1 1 2 
Urophycis chuss Squirrel hake 6 5 6 1 4 
Hippoglossus 

hippoglossus Halibut ?} 1 Z 2 
Pseudopleuronectes 

americanus Flounder 19 3 3 2 15 
Limanda 

ferruginea (?) Sand dab 2 2 2 1 
Total 198 72 70 66 90 


The barn-door skate (Raia stabuliforis) was found to furnish the most 
varied and interesting parasites. Ecto-parasitic on this skate were found; 
Micropharynx parasitica (a tri-clad turbellarian), Aega psora (an isopod), 
and a large leech, Oxyostoma typica.* In the nasal cavity was found 
Charopinus dalmanni (Retz.) a large parasitic copepod. The stomach was 
usually heavily infected with the trematode, Otodistomum cestoides. Large 
numbers of cestodes occurred in the spiral valve. Although only a part 


* For the identification I am indebted to Prof. J. Percy Moore who reports that the 
leeches “‘are representatives of Oxyostoma typica Malm or possibly a closely related species 
of the same genus.” 


10 ILLINOIS BIOLOGICAL MONOGRAPHS [136 


of this cestode material was examined, two forms were identifiéd as 
Rhynchobothrius erinaceus (van Ben.) and Acanthobothrium coronatum 
(Rud.). 

One interesting case of Acanthocephalan infection was found in Fundu- 
lus heteroclitus. The livers of these minnows were almost invariably heavily 
infected with a juvenile form of Neoechinorhynchus. These parasites were 
sometimes free in the liver tissue but usually were coiled in a very thin- 
walled cyst. In one liver 25 or 26 such cysts could be counted. Only two 
of about 25 specimens failed to show the cysts macroscopically. Inonecase, 
this same form of juvenile Acanthocephalan was found in the intestine. 
This possible occurrence of the parasite in the intestine led to feeding 
experiments. A Fundulus was isolated and fed liver containing cysts from 
other minnows. As some of the material was disgorged, it could not be 
ascertained exactly how many cysts were ingested. The fish was fed again 
on the following day, and killed and examined on the third day. Three of 
the Acanthocephala were found in the intestine. This experiment was 
repeated by again feeding an isolated Fundulus the cysts on two days, 
and examining it on the third day. This second fish contained six of the 
Acanthocephala in its intestine. It is evident that the parasite can be 
transmitted from the liver to the intestine of the same species host. 
A possible explanation of the rare occurrence of this type of transfer in 
nature is found in the fact that the viscera of dead minnows in the aquaria 
are readily devoured by the other minnows. No evidence was found that 
the parasite ever reaches sexual maturity in this host. 

The final host of the parasite was found to be the common eel, Anguilla 
chrysypa. The locality from which the minnows were caught harbored 
numerous eels. Two of these fish were caught and examined for parasites. 
The first contained large numbers (about 50) of a Neoechinorhynchus in 
the lower part of the intestine. The parasites were apparently identical 
with the young form taken from the minnow, differing only in beingsexually 
mature. The second eel contained three minnows in the stomach. One of 
these minnows was practically digested. From the stomach content in this 
region one of the Acanthocephalan cysts was recovered. Furthermore, 
there was found free in the upper part of the intestine one of the juvenile 
Acanthocephalans without the cyst. Lower down in the intestine occurred 
large numbers of the adult parasite attached to the intestine wall. The 
species of Acanthocephala was kindly identified by Dr. H. J. Van Cleave 
as Neoechinornynchus cylindratus (Van Cleave). 

The demonstration seems to be quite complete that the eel (at least in 
this particular locality) acquires (at least in part) its infection through the 
minnow, Fundulus heteroclitus. Whether the minnow is a necessary link 
in the life-history of the parasite is very doubtful. Van Cleave (1920) 
in explaining juvenile forms of Acanthocephala encysted in various fish, 


135] SOME NORTH AMERICAN FISH TREMATODES—MANTER 11 


suggests that they may result from ingestion of the larva when it is too 
young to maintain itself in the intestine, the immature larva developing 
to an infective juvenile form in some tissue outside the digestive tract. 

In the course of the present work, no new methods of technique were 
discovered. The finding of the larger parasites such as most cestodes, 
acanthocephala, and nematodes is simple. To collect the smaller forms 
such as many trematodes, the content of the digestive tract of the host 
must be minutely examined. Best results were obtained by diluting a small 
amount of material with considerable water in a large glass dish. A chang- 
ing from light to dark of the background below the dish is often helpful. 
Careful scraping of the wall of the digestive tract is usually necessary to 
remove many of the smaller parasites. 

Cestodes were killed in HgCl: solution. Agitation by shaking or the 
actual stretching by hand of cestodes is necessary to prevent excessive 
contraction. Trematodes were killed according to the Looss method (Looss 
1901) by first shaking in water and then in a 50% solution of HgCl. 
A modified Gilson’s solution (Petrunkevitch solution) was also found very 
satisfactory for trematodes. Nematodes were killed by placing in hot 
70% alcohol or hot Petrunkevitch solution. Acanthocephala from the 
marine fish were first placed in fresh water which causes complete extension 
of the proboscis. When the Acanthocephala no longer respond to stimuli 
they are removed to the killing solution. 

Some difficulty was experienced by some forms, especially trematodes, 
later becoming quite black, due apparently to a precipitation of metallic 
mercury. This condition might be due to insufficient or delayed treatment 
with iodized alcohol. A semisatisfactory method of reclaiming such 
specimens was found to consist of treating them with a weak solution of 
nitric acid. The acid removes the mercury but slightly stains the tissues. 

In staining trematodes for total mounts, Ehrlich’s or Delafield’s 
hematoxylin or a mixture of the two was found to be very satisfactory. 
Alum cochineal also gave good results. Sections were stained with the 
ordinary reagents such as hematoxylin, iron hematoxylin, safranin, eosin, 
orange G, and Lyon’s blue. 

The present studies can be divided into three rather distinct parts as 
follows. First, an intensive study of Otodistomum cestoides, its first larval 
form, its growth changes within the final host, and its morphology. Some 
data was also obtained from an attempt to trace the life history of this 
form. Second, a comparative study of the entire family of the Azygiidae, 
and a revision of the American representatives of the genus Azygia. Third, 
a briefer account of each of the other forms of marine trematodes in the 
collection. This last account also includes data on several forms from the 
collection of Dr. H. B. Ward. These latter were collected from the Woods 
Hole region. 


12 ILLINOIS BIOLOGICAL MONOGRAPHS {138 


HISTORICAL SURVEY 


Van Beneden (1858 and 1871) was one of the earliest workers to deal 
particularly with fish parasites and many of the more common species were 
first described by him. His collections were made along the coast of 
Belgium. Olsson in 1868 records 32 different trematode parasites from 
Scandinavian fish. Twenty-seven of these parasites were distomes, and 
eight were reported as new. Olsson’s work covered a wide host range, 
the trematodes being collected from 42 different species of fish. 

Levinsen published in 1881 results of his studies on trematodes of arctic 
fish. This work is the product of two years spent on the west coast of 
Greenland and constitutes the first comprehensive record of trematodes 
from strictly arctic marine fish. The number of host species examined 
was small (six), but the trematode fauna of a few fish such as the sculpin 
was thoroughly studied. Nine different species of trematodes were recorded 
from this host. Levinsen lists thirteen different sexually mature forms, 
most of which are distomes. Seven species are described as new. 

Early work on the fish trematodes of the Mediterranean was done by 
Rudolphi, Monticelli, Stossich, and Looss. The detailed and accurate 
morphological observations of Looss have been of special service, and his ° 
(1899) conception of the genus among distomes has resulted in a complete 
systematic reorganization of that group. 

Probably the most important paper on trematodes of arctic fish is 
Odhner’s contribution (1905) to the Fauna Arctica, Trematoden des 
arktischen Gebietes. This critical monograph of the arctic trematode fauna 
is not limited to fish parasites but includes a few forms from avian and 
mammalian hosts. Odhner also restudied Levinsen’s material. As the 
paper deals with considerable change in the ‘‘natural system” of trema- 
todes, short descriptions are given of some forms outside the arctic regions. 
Twenty-two different trematodes, 19 of which are Digenea, are recorded 
from fish. Among these fish trematodes, four new genera and three new 
species are described. Several previously known species are redescribed, 
and some important systematic reorganizations are made. In a series of 
later short papers under the general title, Zum naturlichen System der 
digenen Trematoden, Odhner has made numerous subsequent additions to 
our knowledge of relationships among the trematodes, and his conclusions 
have been largely accepted by Nicoll (1915) and others. 

The trematodes of the British marine fish are probably better known 
than those of any other particular region. This is largely due to the re- 
searches of Lebour, Johnstone, T. Scott, A. Scott, and Nicoll. According 


139] SOME NORTH AMERICAN FISH TREMATODES—MANTER 13 


to Nicoll, up to 1915 nearly 100 species of trematodes had been recorded 
from British marine fish. Nicoll’s(1915)list of trematodes from marine 
fish contains 241 different species of trematodes belonging to 119 genera. 
Of these trematodes, 157 species and 73 genera are distomes, 

In America the work of Linton at Woods Hole, Beaufort, N. C., and 
the Tortugas stands almost alone. The last named region is especially 
interesting in revealing a very rich and varied trematode fauna (Linton 
1911) with forms differing considerably from most of the more northern 
forms. Stafford (1904) gives a list of 37 trematodes from 32 different 
Canadian marine fish. Cooper (1915) gives more complete data on a few 
forms from the same region. 

A large amount of the literature is, of course, in the nature of special 
studies on individual or few forms. Examples of papers of this type are 
found in the works of Poirier (1885), Villot (1879), Pratt (1898), Darr 
(1902), Buttel-Reepen (1903), and Miihlschlag (1914). 


14 ILLINOIS BIOLOGICAL MONOGRAPHS {140 


THE MORPHOLOGY OF OTODISTOMUM CESTOIDES 
OTODISTOMUM CESTOIDES (VAN BENEDEN 1871) 


Otodistomum cestoides (van Ben.) 

Syns.: Distomum cestoides van Ben. 1871 
Otiodistomum veliporum of Stafford 1904 
Otiodistomum veliporum of Lebour 1908 
Otiodistomum veliporum of Lénnberg 1891 

From stomach, Raia stabuliforis (=R. laevis) 

Reported hosts: Raia batis 

Raia laevis 

Raia fullonica 

Raia lintea 

Raia clavata 

Raia radiata 

Raia macrorhyncha 
Chlamydoselache anguinea 


Dist. cestoides was first obtained by van Beneden (1871) from Raia batis. 
The genus Otodistomum was named by Stafford (1904) for a form he 
obtained from the stomach of Raia stabuliforis (=R. laevis). This form 
he called Otodistomum veliporum, identifying it as the Dist. veliporum of 
of Creplin. The close resemblance between the two species cestoides and 
veliporum has been a cause of general confusion, and, indeed, the two have 
been considered synonymous. Odhner (1911b) first showed that O. cestoides 
(van Ben.) had been incorrectly identified as O. veliporum by previous 
workers including Stafford, Lebour, and Lénnberg. In the course of the 
present studies both species were available for comparison. Specimens of 
O. veliporum were obtained from the collection of Dr. H. B. Ward* and 
were collected by him from Raia binoculata in Alaska in 1909. Further 
material of this same form was collected by a fellow-student from the 
same host at Friday Harbor, Washington, in 1924. Frequent reference will 
be made to this species in connection with the following discussion of the 
morphology of O. cestoides. 

The host records of the two species are doubtless somewhat confused. 
According to the literature, O. veliporum appears to have a much wider 
host range among the Selachians, O. cestoides being almost entirely re- 
stricted to Raia species. In the region of Mount Desert Island O. cestoides 
occurs abundantly in Raia stabuliforis, but was never found in any other 
species of skate. Both Stafford and Cooper report it from Canadian waters. 


* Collection of Dr. H. B. Ward, vial No. 48a from Excursion Inlet, Alaska, July 22, 1909. 


141] SOME NORTH AMERICAN FISH TREMATODES—MANTER 15 


Linton also records it from Woods Hole but there it seems to be a rare 
parasite. 

The trematode was found in the lower part of the pyloric stomach of 
Raia stabuliforis. It is one of the most common fish trematodes in the 
region of Mount Desert Island as almost all the skates of this species we re- 
infected, sometimes heavily. Only two individuals among twenty examined 
in 1924 were uninfected, while all of the several examined in 1923 contained 
the trematode. The average degree of infection is about 21, although the 
number varies from only 2 or 3 to about 150. In a number of cases only 
young immature forms were found. It is also common, especially if the 
infection is light, to find only mature forms or at least no very young 
specimens, Several instances were found wherein all stages were present. 
Table 2 shows a record of the collection of this parasite. 

The trematode is one of the largest known. Stafford records worms 
as long as 80 mm. when extended. There is a remarkable size variation. 
The longest specimen in the present collection measured about 65 mm., 
while several were found only 2 or 3 mm. in length. Sexual maturity is 
reached when the worm has a length of about 11 mm. 

The body form is elongate and somewhat flattened dorso-ventrally 
especially in the posterior region. The anterior end tapers slightly in front 
of the ventral sucker and is bluntly pointed. Behind the ventral sucker 
the body tapers only very gradually and the posterior end is usually blunt. 
In some cases, however, when the worm is extended the posterior tip is 
sharply pointed. In this case, the body form is spindle-like. 

The two suckers are close together near the anterior end. The ventral 
sucker is the larger and very powerful. When in use this ventral sucker 
may be protruded from the body very prominently. The worms cling 
tenaciously by means of the ventral sucker and may extend the anterior 
end of the body for some distance, feeling about in a leech-like manner. 
When removed from their host the worms cling to each other by means of 
their ventral suckers, and it is often difficult to separate individuals after 
they have become attached in this manner. There is a marked tendency for 
the worms to bend slightly inward, (i.e., ventrad), so that in profile they 
assume a curved or crescentic shape. This shape is especially marked when 
the trematodes are killed unless they are prevented by some mechanical 
means from so curling. The color of the worms is a translucent white when 
alive, becoming opaque white when killed. The region of the uterus just 
posterior to the ventral sucker is dark brown in color, due to the presence 
of many eggs which possess a light brown shell. 

The oral sucker is smaller than the ventral sucker and the size ratio of 
the two does not show any progressive change with growth, averaging the 
same in very small individuals as it does in the largest. The anterior sucker 
averages slightly over .6 the size of the ventral one, or a proportion of 


16 


ILLINOIS BIOLOGICAL MONOGRAPHS [142 


TABLE 2 


InpivipvaL INFECTION OF Raia stabuliforis witTH Otodistomum cestoides 


Date 


July 16 


527. 
August 5 


“ 28 


Content of Stomach | Number of parasites 


Empty 
Sculpin 
Empty 
Empty 


“ 
a“ 
a 
a 


“a 


Crab, shrimp 
Remains of flounder 


3 herring, part of 
lobster 


Empty 


“ 


“a 


8-10 small crabs, 
shrimp 


Empty 


a 


Remains of fish, 
Buccinum 


Flounder 


Several 


4-5 
Many 


None 
12-15 
160-170 


Several 


Z 


Condition 


Mostly mature 


Mature 


Small, immature 


Mature 3 


Small 


All sizes, 10 or more mature 


Mostly mature 


Heaviest infection. 
100 immature 


All sizes 


Mature 


about 3:5. Odhner (1911b), however, gives a ratio of 3 : 4 for O. cestoides 
and 3:5 for O. veliporum. Miss Lebour’s single specimen with a ratio of 
1:2 must have been (as Odhner suggests) an abnormal condition. For 
the measurements of the suckers see Table 4. 

The circular opening of the oral sucker may be directed anteriorly, but 
is usually ventral. The ventral sucker is very deep, extending nearly to 
the dorsal surface of the body when the worm is extended. The cavity of 
this sucker extends posteriorly as well as dorsally, a condition due to the 


143] SOME NORTH AMERICAN FISH TREMATODES—MANTER 17 


greater development of its muscles in the posterior region. While interest- 
ing because of the high degree of muscular development, the structure of 
the two suckers is like that already described for similar forms by Poirier 
(1885) and for O. veliporum by Miihlschlag (1914). 

From the ventral anterior rim of the ventral sucker two muscle bands 
pass dorsally and can be traced nearly to the longitudinal body muscles 
of the dorsal wall. Crossing them obliquely a strong band of muscles can 
be seen to extend ventrally and anteriorly from the central dorsal border 
of the sucker to the longitudinal muscles of the ventral body wall. There 
are also muscle fibers extending laterally from this anterior ventral border 
of the sucker. Muscle bands at the posterior border of the sucker extend 
laterally on each side, and other bands extend dorsally to the dorsal body 
wall. : 

Short muscles are attached to the anterior margin of the oral sucker 
and course anteriorly and dorsally where they seem to join longitudinal 
body muscles of the dorsal side. Just posterior to these occur lateral oblique 
muscles running dorsally and laterally from each side of the sucker. They 
also are closely related with the dorsal longitudinal body muscles. Some 
of these fibers extend to the outer edge of the sucker, Finally, from the 
posterior edge of the sucker oblique muscle bands run dorsally and pos- 
teriorly and attach themselves to the pharynx. 

The body wall consists of the cuticula, a layer of circular muscles, and 
a layer of longitudinal muscles (Fig.12). The cuticula is a thick structureless 
layer surrounding the entire body. In a specimen about 25 mm. in length, 
this cuticula was about 17y thick on the ventral surface of the neck region 
and about 28 thick on the ventral surface of the posterior region. The 
thicknesses on the dorsal surfaces of the same regions were 34 and 37y, 
Hence, the same relative thicknesses are found that Mihlschlag noted for 
O. veliporum. For the latter species, Miihlschlag’s measurements are all 
much smaller than were found in the present species, but the size of the 
specimen was not given in the former case. The cuticula is much thinner 
over the inner surfaces of the two suckers. Here it measures only 5 to 8y 
in thickness. 

The body wall is thrown into circular folds which are more prominent 
with increased degree of contraction. These folds give the ringed appear- 
ance characteristic of this group of trematodes. Sections show that these 
folds involve the cuticula, and the layer of circular muscles, but not the 
layer of longitudinal muscles. The thickness of the circular layer, therefore, 
varies greatly. The layer is very thick in the center of the folds, and is 
greatly reduced in the furrows between the folds. In the following table 
a medium condition is represented as far as possible. 


18 ILLINOIS BIOLOGICAL MONOGRAPHS [144 


THICKNESS OF REGIONS OF Bopy WALL 
(Specimen about 25 mm. long) 


Ventral Surface 


Neck Region Testis Region Posterior Region 
Cuticula 17 og 28-30u 28-30 
Circular muscles 40-50 50-55 50-55 
Longitudinal muscles 34 17-20 17 
Dorsal Surface 

Cuticula 340 40 wu 35-45 
Circular muscles 50 50 38 
Longitudinal muscles 22 20 16 


The parenchyma presents no unusual features. It consists of a spongy 
tissue, filling in the regions between organs. Small nuclei are common, and 
also larger cells which are possibly nervous in function. The parenchyma 
is set through with muscle bands. Many of these, especially near the body 
wall, and within the neck region are oblique or diagonal, but the majority 
run in longitudinal bands throughout the length of the body. In species 
of Azygia (a related genus) a very definite and relatively narrow band of 
these longitudinal muscles occurs. In cross-section, the body is separated 
by them into medullary and cortical regions. Various Azygia species were 
available for comparison with O. cestoides in this respect. The localization 
of the muscles is much more pronounced and definite in Azygia where they 
form a rather compact layer. Here also the follicles of the vitellaria are 
outside this layer, that is, in the cortical region. In Otodistomum, the 
longitudinal parenchyma muscles are not limited to such a narrow layer 
and their formation is much less compact (Fig. 23). The region of their 
occurrence is, however, definite enough so that it can be noted that the 
follicles of the vitellaria lie largely internal to them, a condition to be 
contrasted with that occurring in Azygia species. 

The nervous system could not be worked out in detail, only its more 
prominent features being noted. These agreed with data already known 
for similar forms. 

The pharynx is ovoid or egg-shaped. It is located just posterior and 
slightly dorsal to the oral sucker. Its size is about 0.5 mm. by 0.3 to 0.4 
mm. in average sized specimens. The largest examples measured about 
0.75 mm. in length. Ina specimen 24.5 mm. in length the pharynx measured 
0.56 by 0.37 mm., and the thickness of its walls was about 0.18 mm. There 
is no pre-pharynx and the pharynx itself may protrude slightly into the 
cavity of the oral sucker. The pharynx usually extends obliquely dorsally 
and posteriorly. The opening between pharynx and oral sucker is therefore 
facing obliquely between a dorso-ventral and a posterio-anterior direction. 
The walls of the pharynx are very muscular and show the same sets of 
muscles found in the suckers. Circular or equatorial muscles are especially 


145] SOME NORTH AMERICAN FISH TREMATODES—MANTER 19 


powerful in the posterior region where the esophagus joins the pharynx and 
these may act as a sphincter muscle between the two (Fig. 10). 

Special muscle bands run obliquely forward from the dorsal and ventral 
sides of the pharynx to the oral sucker. These bands are much more 
prominent on the ventral side. The degree of contraction of these muscles 
no doubt accounts for the varying position of the pharynx especially its tip 
in the dorso-ventral direction in relation to the oral sucker. Sometimes 
the pharynx entirely overlaps the sucker dorsally and rarely it extends 
almost directly posteriorly. 

The pharynx leads directly into the esophagus. In a specimen about 
25 mm. long the anterio-posterior length of the unpaired region of the 
esophagus adjacent to the pharynx is only about 57, but the organ divides 
immediately into two lateral stems and is actually a tube running laterally 
and perpendicular to the long axis of the pharynx. The length of each 
lateral stem is about 0.4 mm. Each stem bends toward the anterior and 
extends in that direction about 0.3 mm. before opening into the intestine 
proper (Fig. 10). The esophagus lies dorsal and partly lateral to the 
pharynx. 

Outside the cuticula layer of the esophagus occurs a layer of circular 
muscles covered in turn by a thin coat of longitudinal muscles. The 
circular muscles are more prominent in the region where the esophagus 
joins the intestine, and serve here as a sphincter muscle usually giving rise 
to a slight constriction in this region. Usually at about the level of the 
middle of the pharynx the esophageal stems on each side open into the 
ceca of the intestine proper. The internal cuticular layer of the esophagus 
ends abruptly at this point (Fig. 10). The intestinal ceca continue forward 
for a short distance, then bend abruptly and lead posteriorly. 

The intestine shows no special regions. The two branches stretch nearly 
to the posterior tip of the body. They spread apart in the region of the 
ventral sucker, but approach each other closely immediately posterior to 
the sucker. They are also forced somewhat laterally by the ovary and 
testes. Just behind the posterior testis they again approach each other 
slightly. As in other related trematodes (Azygia and Leuceruthrus), the 
ceca are thrown into small folds throughout their length, the folds being 
more pronounced the higher the degree of body contraction. Each branch 
of the intestine ends blindly. There may be a slight difference in their 
length. That no significance can be attached to the frequently unequal 
length of the ceca is shown by the fact that the right is sometimes longer 
and sometimes shorter than the left. 

The intestine is lined internally by a layer of cuboid or low cylindrical 
cells from which long wavy protoplasmic processes stream out into the 
lumen usually nearly filling it (Fig. 10). The internal boundary of these 
intestinal cells is very indefinite. The size of the cells is the same in very 


20 ILLINOIS BIOLOGICAL MONOGRAPHS [140 


small specimens and in the largest. A thin membrane surrounds the 
intestine which is also provided with a thin circular (internal) and longi- 
tudinal (external) muscle layers. 

The excretory system is like that of similar forms. It consists posteriorly 
of a large single median tube which may be much swollen, lying between 
the branches of the intestine, and opening by means of a short duct at the 
posterior tip of the body. This tube branches a short distance behind the 
posterior testis, its two branches crossing the intestinal ceca ventrally and 
proceeding anteriorly lateral to these ceca. The two branches are con- 
tinuous anterior to the oral sucker.. The main excretory system consists 
then, of a Y-shaped tube with the two forks of the Y continuous. This tube 
may be thrown into folds comparable with those described for the intestine. 
Its outline in cross-section is very irregular and it can be seen to be con- 
tinually receiving minute lateral branches. Its thin membraneous lining 
is obscured by many deeply staining spherical granules which thickly 
adhere to the wall of the main tube throughout its length. These con- 
cretions are generally considered as waste products, and are commonly 
known in many trematodes. , 

Flame cells are numerous. They are small cells oval in shape, with 
prominent nuclei. Favorable sections show that they occupy ends of minute 
excretory ducts and that their tips are prolonged into a tuft of cilia about 
equal to the cell body in length. The cells measure about 14 by 8p. 

The genital pore is ventral, median, between the two suckers and much 
closer te the oral sucker. It leads into a roomy genital atrium within which 
usually projects the nipple-shaped genital cone or papilla (Fig. 5). Both 
the genital atrium and the papilla are lined with cuticula which, however, 
becomes very thin at the tip of the cone. Just beneath this cuticula the 
wall of the atrium is strengthened by a thick layer of circular muscles. 
These muscles continue about the base of the papilla but gradually dis- 
appear toward its tip. Outside these circular muscles is a layer of longi- 
tudinal muscles, that is, muscles running in the direction of the long axis 
of the papilla. These muscles are continuous from the wall of the atrium 
into the papilla where they are internal to the circular muscles. Oblique 
muscles run off from the region of the longitudinal muscle layer of the 
atrium. In the solid-appearing tissue of the cone occur numerous nuclei 
which are more numerous near the tip of the papilla. 

What at first appeared to be a marked difference in the size and occur- 
rence of this papilla in the two species of Otodistomum led to a study of 
the permanency and variability of this organ. In the related genus Azygia, 
the genital atrium is usually without a papilla, the common sex duct 
opening at its base. This base of the atrium is, however, protrusible so 
that it can be thrust out papilla-like. Thus, here the genital papilla is only 
a momentary or temporary structure. Odhner (1911b: 518) says in 


~ 147) SOME NORTH AMERICAN FISH TREMATODES—MANTER 21 


regard to this condition; ‘‘Dies konnte den Verdacht erwecken, dass es sich 
bei Otodistomum am Ende in derselben Weise verhielte; doch scheint mir 
dort die Papille einen mehr ‘soliden’ Eindruck zu machen.” 

Sections through O. veliporum from the Pacific showed the genital 
papilla almost always entirely absent or quite rudimentary in size. In 
O. cestoides the papilla was usually of robust form filling most of the atrium, 
or even entirely protruded from it (Fig. 6). In the latter case, the atrium 
itself is practically eliminated. In order to determine the constancy of 
the papilla, specimens of various sizes and degrees of body contraction 
were sectioned. Specimens collected in different years and killed in different 
solutions were also compared. The usual and contrasting conditions found 
are represented in Fig. 8 (O. cestoides) and Fig. 7 (O. veliporum). Of the 
specimens of O. veliporum sectioned, six showed the papilla absent, or a 
condition as in Azygia, three showed a small papilla (Fig. 7), while one 
showed a prominent papilla partially protruded from the pore (Fig. 29). 
Among eight specimens of O. cestoides sectioned, one showed the papilla 
entirely protruded (Fig. 6), six showed a robust papilla largely filling the 
genital atrium (Figs. 5 and 8), while one showed the papilla entirely 
absent (Fig. 28). Odhner’s suspicion is therefore correct. Although the 
genital papilla has always been described and figured as a prominent feature 
in Otodistomum species it is capable of being entirely withdrawn as is 
normally the condition in Azygia. What appeared, then, to be a clear 
distinction between the two forms studied becomes a weak taxonomic 
character since it is variable and inconstant. 

The atrium in O. veliporum from the Pacific almost constantly led very 
sharply posteriad and only slightly dorsad, while in the Atlantic form 
(O. cestoides) the slope of the atrium was almost directly dorsad and only 
slightly posteriad. This degree of slope of the atrium is probably associated 
with the condition of the papilla as when this structure was completely 
withdrawn in O. cestoides the atrium led sharply posteriad (Fig. 28). 

Measurements on the size of the atrium and papilla in different speci- 
mens are as follows: 


Otodistomum veliporum 


Genital atrium Genital cone 
1. 0.845 0.093 mm. 0.102 by 0.08 mm. 
2. 0.9 by 0.06 0.075 0.035 
3. 0.935 0.112 absent 
4. 0.935 0.168 0.056 0.093 
5. 0.935 0.149 absent 
6. 2.04 0.32 absent 
de Andi] 0.3 absent 
8. 1.57 0.28 absent 
9. 1.25 0.23 absent 
10. 0.9 0.5 1.25 0.43 


22 ILLINOIS BIOLOGICAL MONOGRAPHS [148 


Olodistomum cestoides 


Genital atrium Genital cone 
1. 0.243 X& 0.187 mm. 0.168 X& 0.149 mm. 
2. absent 0.71 0.52 
35/0233 0.28 0.28 0.2 
4. 0.617 0.355 0.317 0.317 
5. 0.37 0.187 0.187 0.187 
6. 0.6 0.6 0.39 0.54 
7. 0.94 0.62 0.39 0.54 
8; 1.25 O15 absent 


It is certain that the size of the papilla is independent of general body 
contraction. Measurements No. 4 in the above table represent a strongly 
contracted specimen of O. veliporwm and an extended specimen of O. 
cestoides. The size of this structure is also independent of the killing fluid. 
Sometimes the body wall projects lip-like about the genital pore. This 
condition also is not associated with the size of the papilla. A definite 
system of muscles about the papilla and in the neck region seems to be 
responsible for the protrusion and withdrawal of the papilla. 

The exact mechanism for the protruding of the papilla is difficult to 
determine and probably depends upon a rather complex system of muscles. 
The longitudinal muscles about the wall of the atrium have processes 
which attach themselves to the anterior (or ventral) part of the atrium 
(Fig. 28). At the other end these muscles are continuous with the longi- 
tudinal body muscles. Contraction of these muscles of the atrium would 
have a tendency to widen and to pull forward the anterior part of the 
atrium. The actual pushing out of the base of the atrium to form the 
papilla is probably brought about by the numerous diagonal and dorso- 
ventral muscles of the neck region. Contraction of these muscles causing a 
compression of body tissue in that region would provide a pushing force 
at the base of the atrium. Once the movement of the extrusion has started, 
it would be aided by the contraction of the circular muscles in the wall of 
the atrium and base of the papilla. Of the two specimens with papilla 
protruded O. cestoides showed the ejaculatory duct somewhat coiled even 
in the papilla itself, while this duct was straight in the papilla of O. veli- 
porum. The duct is always coiled between the cirrus sac and the papilla, 
and in unprotruded papillae. The sudden projection of sperm and seminal 
fluids through this muscular duct would have a tendency to straighten 
its coiled condition just as such an effect is brought about by sudden 
pressure of water in a coiled hose. This influence is, of course, an uncertain 
one in this case and even if present would probably have a negligible effect 
in elongating the papilla. The retraction of the papilla doubtless results 
from the contraction of the longitudinal muscles which it possesses. 

The papilla probably functions as a copulatory organ. In the specimen 
of O. veliporum with protruded papilla (Fig. 29), a large mass of sperma- 


149] SOME NORTH AMERICAN FISH TREMATODES—MANTER 23 


tozoa was emerging from the genital duct at the tip of the papilla. Sperma- 
tozoa were also found crowding the distal tip of the vagina for a short 
distance, as well as in the genital atrium outside the papilla. None were 
found in the vagina posterior to the papilla. Eggs were frequently found 
in the atrium but only when the papilla was completely withdrawn, a 
fact which indicates that egg laying occurs while the papilla is completely 
subsided. 

The two testes lie one immediately behind the other in the median line 
at about the center of the body. They are close together and very com- 
monly are in contact with each other. This condition depends, however, 
upon the state of body contraction. The posterior testis is always slightly 
larger than the anterior testis. Each testis is surrounded by a fibrous-like 
membrane containing a few flattened nuclei. In adult forms from the 
Atlantic collection (O. cestoides) the size of the anterior testis was 0.62 to 
1.25 mm. by 0.8 to 1.12 mm., while the posterior testis measured 0.8 to 
1.37 mm. by 0.8 to 1.2 mm. The organs seemed to be rather consistently 
somewhat larger in O. veliporum. 

The duct from the anterior testis leads from the ventral side of that 
organ near its anterior end, and extends anteriorly in the right half of the 
body. The other male duct leads from the ventral side of the posterior 
testis about 1/4 the length of the organ from its anterior end. Thus, in the 
specimen studied, the posterior testis measured 1.235 mm. and the duct 
opened 0.365 mm. from the anterior end. This condition may be at least 
’ partially due to the angle at which the sections were cut. The duct from 
the posterior testis leads anteriorly in the left half of the body. Both ducts 
at first lie ventral to the uterus but like the uterus pass dorsal to the ventral 
sucker, and in this region they also gradually become dorsal to the uterus. 
Slightly anterior to the posterior margin of the cirrus sac both ducts swing 
ventrally. The two do not unite until just before they empty into the 
seminal vesicle. Relations of the ducts were found to be the same in both 
O. cestoides and O. veliporum. Miihlschlag, however, gives the ducts as 
arising from the median anterior borders of the testes and uniting into a 
common duct dorsal to the cirrus sac. The diameter of the vas deferens 
varies but when expanded measures 26 to 39u with a very thin mem- 
braneous wall except in regions where the wall expands into prominent 
cells. (Fig. 25.) 

The cirrus sac is large and elongate-ovoid in shape. It lies between the 
two suckers somewhat nearer the oral. In average sized specimens (23 to 
35 mm.) it measures 0.84 to 1.02 mm. by 0.65 to 0.84 mm. It may attain 
a length of 1.3 mm. It is somewhat larger in O. veliporum where it reaches 
a length of 1.4 mm. The sac is definitely bounded by a thin membrane 
about which is an inconspicuous coat of circular muscles. Both seminal 
vesicle and prostate gland are contained entirely within the sac. 


24 ILLINOIS BIOLOGICAL MONOGRAPHS {150 


The seminal vesicle is a large swollen tube almost filling the posterior 
half of the cirrus sac. It is somewhat curved in shape and always packed 
with sperm cells. The sperm cells are thread-like in form with minute 
round heads. The wall of the vesicle is made up of flattened cells with 
large nuclei. The pars prostatica of the male duct leads from the anterior 
end of the seminal vesicle, proceeds posteriorly and dorsally, then bends 
anteriorly and runs diagonally forward to the anterior end of the cirrus 
sac. It is surrounded by the large prostate gland which fills the remainder 
of the cirrus sac. Just before the duct leaves the cirrus sac its character 
changes very abruptly into that of the ejaculatory duct. 

The ejaculatory duct follows a much winding course leading to the 
tip of the genital papilla. Distally, it is joined ventrally by the vagina. 
The coiling of the duct in O. cestoides continues in the genital cone itself 
even when the latter is fully extended. The duct is lined by a thick layer 
of cuticula-like material continuous with the body cuticula. This layer 
attains a thickness of 10 to 134 and shows a folded irregular outline in 
cross-section. It is surrounded by a thick coat of circular muscles which 
becomes 20 to 25u in thickness near the cirrus sac. No longitudinal muscles 
could be noted. 

In development the male reproductive system precedes that of the 
female. The seminal vesicle is filled with sperm cells some time before eggs 
appear in the uterus and before the vitellaria appear at all. 

The ovary lies immediately in front of the anterior testis and usually 
in contact with it. In both organs the surface of contact is somewhat 
flattened. The ovary is therefore flattened on its posterior surface and its 
longest dimension is in the right and left direction. It may lie a little to 
one side of the testis, either to the right or to the left. (Figs. 13 to 18.) 
Its position in this respect is very inconstant and the various descriptions 
of the position of the ovary in this and similar forms is probably without 
significance. It is normally almost directly in front of the anterior testis. 
The size of the ovary in fully mature forms is 0.43 to 0.6 mm. by 0.78 to 
0.9 mm. It is slightly larger in O. veliporum where it reaches 0.8 by 1 mm. 

The ootype lies immediately anterior and slightly dorsal to the ovary 
with which it is in close contact. Both organs are surrounded by a common 
fibrous tissue which also separates the two. The ootype is somewhat smaller 
than the ovary. In an average sized specimen where the ovary measured 
0.5 by 0.84 mm., the ootype measured 0.35 by 0.53 mm. 

The oviduct leads from the middle anterior aspect of the ovary. It 
projects into the ovary in the form of a funnel-like structure with thick 
walls. This condition was found in both species (Fig. 11). The walls are 
composed of fibrous tissue which is continuous with the tissue covering 
the ovary and the ootype. This tissue is quite thick between ovary and 
ootype, and in it occur the two lateral vitelline ducts. As these ducts 


151] SOME NORTH AMERICAN FISH TREMATODES—MANTER 25 


approach each other they also tend to encroach upon the ootype so that 
they give the impression of pushing into it from the rear. Since the fibrous 
lining tissue becomes very thin between the yolk duct and the cells of the 
ootype, it is difficult to determine the exact point of penetration of the 
ootype by the yolk duct on either side. Frontal sections of O. cestoides 
indicate that the lateral ducts may penetrate the ootype before uniting 
to form the common yolk duct. More commonly, however, the two lateral 
ducts unite while still within the fibrous tissue close to the ootype and 
only the common duct actually penetrates into that organ. 

Almost immediately after entering the ootype proper the oviduct is 
joined by the common vitelline duct and by Laurer’s canal. The common 
vitelline duct is very short. A rather unusual condition was found in at 
least two cases where Laurer’s canal instead of joining the oviduct opened 
at the point of union of the two yolk ducts, so that the three canals opened 
together into the oviduct (Fig. 24). In other cases noted, Laurer’s canal 
was slightly to the right and appeared to join the right vitelline duct. 
Again, Laurer’s canal may join the oviduct at about the same point as 
does the common yolk duct. 

Laurer’s canal is very well developed. It is lined with cuticula 4 to 64 
in thickness. In medium-sized specimens the duct is about 25y in diameter. 
A circular layer of muscles surrounds it but no special longitudinal muscles 
could be made out. The tube is much coiled and leads dorsally and either 
anteriorly or posteriorly as will be shown later. Within the lumen of the 
canal are many sperm cells. In some cases, in the region adjacent the 
oviduct a few yolk cells were noted. A seminal receptacle is absent. 

After receiving the yolk duct and Laurer’s canal, the oviduct, now the 
uterus, becomes a small tube only about 26y in diameter with a thick wall 
made up of very definite cells with large nuclei. Into the lumen of this 
tube project cilia-like processes. The tube very shortly enlarges and the 
nature of its wall becomes one of large cuboidal and heavily granular cells 
(13 to 23u in thickness). This part of the tube coils about more or less 
within the ootype for a short time and continues also outside of that organ. 

All stages in formation of the egg shell can be traced from the point 
where the yolk duct joins the oviduct. The shell material can be first seen 
as a shapeless irregular mass surrounding an egg cell and a group of yolk 
cells. Within the cellular-walled uterus region the eggs still lack their 
characteristic shape. The inner surface of the forming shell often shows 
vacuole-like spaces (Fig. 26). The cellular region of the uterus as it coils 
anteriorly soon passes over into a region characterized by a thin simple 
membraneous wall. By the time the eggs have reached this region they 
possess hardened and fully formed shells. 

The uterus contains thousands of eggs and extends anteriorly in many 
transverse coils. It passes dorsal to the ventral sucker and ventral to the 


26 ILLINOIS BIOLOGICAL MONOGRAPHS [152 


seminal vesicle. At about the level of the ventral sucker it becomes less 
coiled and the nature of its wall changes to produce a region which may 
be called the vagina. 

The vagina like the male ejaculatory duct is lined internally by cuticula. 
It possesses two layers of conspicuous muscles, an inner circular layer and 
an outer longitudinal layer. The vagina contains few eggs and above the 
ventral sucker is almost a straight tube. It leads to near the tip of the 
genital cone where it unites with the male ejaculatory duct. There is 
a common duct for a distance of about 25. 

In development the uterus first appears as a solid string of cells without 
a lumen. Sections of a very young specimen seem to show a lumen appear- 
ing first within the ootype the start of which appears early with the 
beginning of the ovary. It is an interesting fact that in slightly older 
specimens when the uterus can first be made out in toto-mounts but before 
eggs are being produced, this string-like beginning of the uterus assumes 
the coiling which characterizes the organ when filled with eggs. It winds 
transversely back and forth between the ovary and ventral sucker, crossing 
the body as many as 40 to 50 times, approximately the same es ceetce of 
folding that is found in the adult. 

The first eggs to be produced are abortive. A specimen 11.5 mm. in 
length showed the earliest egg still in the region of the ventral sucker. 
The most anterior eggs (15 to 20) were only about half the size of the others 
and were almost spherical with very thin shells. They measured from 22.8 
to about 30u, the smallest being most anterior. The eggs nearer the ovary 
were larger but still showed a very thin shell, in striking contrast to the 
thick shell found in the adult egg. No eggs in this specimen measured over 
68, a measurement slightly below the average adult size. 

The vitellaria are interesting because of the variation of their extent 
and arrangement. They are of the follicular type and consist of separate 
spherical bodies grouped in two longitudinal rows along the sides of the 
body. The follicles lie mostly ventral to the digestive system. They do 
not appear until relatively late in development, or just before eggs begin 
to be formed. At this time the follicles are very small, approximately the 
size of the eggs (about 50u in diameter), but in the adult they reach a 
diameter of 150 to 190u. Several hundred of these follicles are connected 
by ducts which unite into a common lateral duct on each side at the level 
of the ootype, and these two lateral ducts unite in the ootype as described. 
The rows of follicles are usually narrow, but the width of the rows often 
increases to such an extent that the two approach each other medianly. 
Thus, Miss Lebour (1908) figures the vitellaria massed together posterior 
to the testes. Such variations are not common, however, the two rows 
being usually distinctly separate. Irregular breaks or spaces free of follicles 
are common, and certainly can have no specific significance within the 


153] SOME NORTH AMERICAN FISH TREMATODES—MANTER 27 


genus Otodistomum. Even the differences in the vitellaria given by 
Odhner (1911b) to distinguish O. cestoides from O. veliporum are quite 
useless. He gives the vitellaria in O. veliporum as beginning behind the 
middle of the uterus and as being compressed into narrow rows, while in 


TABLE 3 


VARIATION IN POSTERIOR EXTENT OF VITELLARIA IN O. cestoides 


Body length | Distance from Extent of right Extent of left 
posterior testis to} vitellaria beyond | vitellaria beyond b b 
posterior tip posterior testis posterior testis C ei 
a b G d 
31. mm. 16. mm. 6.4 mm. 7.6 mm. <o 2.1 
38. 21 12.8 13.2 1.6 i) 
24.5 13:5 crosses over to left 7.9 17 i Lf 
side 

20. 8.3 8.3 T3 1. 1.1 
28. 13.5 10.6 9.8 2 133 
1G 7.5 5.6 6.25 1.3 1,2 
19, 9 4.8 Sah 1.8 2.4 
29. 14 both unite in center 8.4 1.6 1.6 
38. 18 9.3 12.41 1.9 1.4 
16. 8. 4. 4.6 127 7 
18. 8. 5:5 ed 1.4 1.1 
16. 6 both unite in center Ss 152 1.2 
11. 5:3 2.9 2.9 1.8 1.8 
10.5 5 2.4 Jnl Zt 1.6 
10.8 5 353 35 155 1.6 
10.5 5 Blew | ih 1.3 1:3 
11.5 6. 3.9 3.9 LS 1.5 
alle 5.3 25 2.5 Pea | 2.1 
26. 10.5 7.4 7.2 1.4 1.4 
26. 14. united for 2.8 mm. 8.7 1.6 1.6 
28. 15. 6. 6. 25 2.5 
Si. 17. unites with left 7.4 222 2.2 
28. 13; unites with left 8.7 155 Ds5 
28. 152 6. 6. 2:5 2:5 
29. tS: 9.4 9.4 15) 1.5 
32). 16. 8.2 10.7 1.9 1.25 


O. cestoides the follicles ordinarily begin in front of the middle of the uterus 
and are not as compressed. This distinction cannot be maintained. In 
O. cestoides, while the vitellaria have their anterior limit between the ovary 
and ventral sucker, approximately half way between these two organs, 
they may extend clearly beyond this mid-uterine point or may fail to 
reach it by some distance. 

Posteriorly, the vitellaria always extend considerably beyond the 
posterior testis and practically always reach at least half the distance 


28 ILLINOIS BIOLOGICAL MONOGRAPHS {154 


between the hind testis and the posterior end of the body. Two cases (one 
in O. veliporum and one in O. cestoides) were noted wherein the vitellaria 
extended to the extreme posterior tip of the body. One row of the follicles 
may be several millimeters longer than the other. The rows may unite 
and run together for several millimeters either medianly or on one side. 
As such variation in these organs is unusual a table has been prepared to 
show more detailed measurements (Table 3). 

The average egg size for O. cestoides was 69.4 by 46.2u as derived from 
over 50 measurements. This size agrees with data by Odhner (1911b) who 
gives 0.065 to 0.072 by 0.043 mm., and Cooper (1915) who gives 0.070 by 
0.042 mm. The thickness of the egg shell measured under oil immersion 
lens averaged about 4.5u. This thickness is somewhat above the measure- 
ments of Odhner, who gives 0.003 mm. and Cooper, who gives 0.0028 mm. 
The eggs of O. veliporum averaged 85.5 by 57.8u. 


” 


155] SOME NORTH AMERICAN FISH TREMATODES—MANTER 29 


GROWTH CHANGES IN OTODISTOMUM CESTOIDES 
WITHIN THE FINAL HOST 


Since it is clear that the trematodes must be slightly under 2 mm. in 
length when first entering the skate, there is a growth within that host to 
about 40 times. Moreover, the parasite increases its size by six or seven 
times after it has become sexually mature. This growth of the worm within 
the skate is marked not only by degree, but also by a regional localization, 
which results in very different conditions of body proportions in the young 
and in the adult. The growth is largely in the region posterior to the ventral 
sucker, and consists mostly in body elongation. 

A study was made of this localized growth and its effects upon various 
body proportions. The material at hand was especially favorable for such 
study not only because the extremes in size were conspicuous, but also 
because all intermediate sizes were available. 

Regional growth in trematodes has been noted in a general way by 
various workers. Braun (1894:567) says of trematodes in general: ‘‘— junge 
Exemplare sind nicht nur absolut, sondern auch relativ kiirzer, indem 
besonders das hintre Kérperende mit der Entwicklung der Geschlecht- 
sorgane bedeutend an Linge zunehmen kann. Gleichzeitig treten auch 
andre Veranderingen der Gestalt auf, die so bedeutend sind, dass es oft 
der Uebergangsstadien bedarf, um eine Jugendform zu diagnosticiren.” 

As early as 1870 van Beneden stated that the young form of Dist. 
hispidium was entirely different from the adult. 

A proportionally greater increase in length than in width was indicated 
by von Linstow (1890) for Dist. cylindraceum, but only a few forms were 
measured. Specimens measured were 4.5 by 1.4 mm., 6-7 by 1.5 mm., and 
13 by 2 mm. 

The liver fluke (F. hepatica) shows a very marked increase of the 
posterior regions at the time of sexual maturity as shown by both Thomas 
(1883) and Leuckart (1886). This growth change also affects the ventral 
sucker which increases its size ratio to the oral sucker. Thus, according to 
Thomas (1883:132) the suckers are of nearly equal size in the cercaria 
while in the adult the diameters of the oral and the ventral suckers have 
the ratio 1:1.35. In F. hepatica the body form also increases rapidly in 
width. 

Barlow (1923) gives measurements of hundreds of individuals of 
Fasciolopsis buski. While the size changes in this form are interesting, there 
does not appear to be conspicuous changes in proportions. 


30 ILLINOIS BIOLOGICAL MONOGRAPHS (156 


Cort (1921) has given the changes in body proportions with growth in 
Schistosoma japonicum. It is interesting that these changes parallel very 
closely the changes in O. cestoides, an entirely unrelated form. Like the 
fish trematode, the adult blood fluke is elongate, whereas the young are 
short and wide. The adult Schistosoma japonicum may increase its size 
as many as 100 times over that of the cercaria. The changes “‘consist in a 
very great increase of the length in ratio to the width, an enormous increase 
of the post-acetabular region of the body as compared with the pre- 
acetabular, and a gradual assumption of the secondary sexual character- 
istics which produce the sexual dimorphism of the adult.”” Especially 
interesting are changes in the size ratio between the two suckers. ‘In the 
cercaria the ventral sucker is only about 1/3 the diameter of the oral 
sucker. In an early stage of development, the suckers become about equal 
in size, and in later stages the ventral sucker is constantly larger than the 
oral sucker.” This progressive change in sucker ratio is to be contrasted 
with the constancy of this ratio in O. cestoides as will be shown later. 

Growth phenomena have been noticed in the Azygia group by Ward 
(1910) for A. sebago and by Miihlschlag (1914) for Otodistomum veliporwm. 
Ward says (of A. sebago): ‘‘The anterior region assumes the form of an 
ellipse surrounding the two suckers. This region changes relatively little 
in size with growth. In one of the smallest specimens (measuring 1.6 mm.) 
the distance between the centers of the two suckers was 0.5 mm. In one 
10 mm. long, this distance measured 1 mm.’ Miihlschlag found by 
measuring the largest and smallest specimen of his collection of Otodistomum 
veliporum that the neck region compared with the body region was 1:4 
in the young forms and 1:7.8 in the largest individual. He concludes: 
“dass bei verschiedener Grisse der Tiere der Hinterkérper relativ stairker 
wichst als der Vorderkoérper.”’ 

In Otodistomum cestoides the contrast in form between a very young 
and a sexually mature individual can be seen by comparing Fig. 1 and 
Fig. 2. Measurements were made on over 200 specimens varying in size 
from 2.3 mm. to65 mm. The measurements (taken on alcoholic specimens) 
included length, width at broadest point, and distance from anterior end 
to the posterior margin of the opening of the ventral sucker. The margin 
of the opening was chosen because the outline of the ventral sucker itself 
is usually not distinct in unmounted specimens. The position of the opening 
varies somewhat in relation to the outline of the sucker, but, in general, 
approximates very constantly the true position of the sucker. All measure- 
ments can be considered only as approximate as most were taken with a 
millimeter rule which necessitated estimations of half and quarter milli- 
meters. The smaller specimens were measured microscopically. 

The youngest specimens (which very probably represent the earliest 
condition in the skate) are strikingly unlike the adult in body proportions. 


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159] SOME NORTH AMERICAN FISH TREMATODES—MANTER 33 


Thus, in individuals 2 or 3 mm. in length the ventral sucker is located 
just anterior to the center of the body, the proportion of the region in 
advance of the posterior border of the sucker to the entire body length 
being 1: 2.3, 1:2.5, 1:3, etc. (see Chart 1). As the trematodes increase 
in size, the region posterior to the ventral sucker gradually and constantly 
gains in size in proportion to the anterior region, which grows relatively 
little. This change can be followed in the accompanying chart (Chart 1) 
on which the body lengths and positions of the ventral suckers have been 
plotted. The total length in half millimeters is plotted on the vertical lines 
as is also the position of the ventral sucker. Each vertical line, then, repre- 
sents one trematode so that if the base line be considered as the anterior 
ends of the worms, the points where the lower curve intersects the vertical 
lines represent the positions of the ventral suckers, while the upper curve 
represents the posterior ends of the trematodes. Ten specimens are repre- 
sented between two successive verical lines. The change in proportion 
and the constancy of the change can be seen at a glance. 

The fluctuations in the lower curve are due to differences in contraction 
of individual specimens. Because of such differences the chart can only be 
considered as approximate. Quite a number of the specimens were stretched 
slightly by hand when killed in order to prevent contraction. Separate 
tables and charts were prepared, however, for individuals not so treated, 
and in every case results were the same as in the complete table of all 
individuals. In the collection of material numerous of the more mature 
trematodes were destroyed for the purpose of obtaining eggs. Without 
doubt, the only change which would be caused in the chart by such loss 
would be to reduce the degree of incline or steepness of the upper curve in 
the region above horizontal line 50 or 60. 

Study of the data on length and width of the trematode at different 
stages showed corresponding results. The measurements are plotted in 
Chart 2 where it can be seen that increase in width is very little in com- 
parison with increase in length. The elongate form which gives the adult 
worm a cestode-like appearance is only gradually assumed with age, and 
the youngest individuals are very characteristically trematode-shaped. 
In Chart 2 the distance on any vertical line from the point of intersection 
of the lower curve to the base line represents the width of an individual 
specimen whose length is represented by the distance from the upper curve 
to the base line. As the specimens are arranged in order of length, here 
again all fluctuations due to varying degrees of contraction appear in the 
lower curve only. 

In spite of these radical] changes in body proportions, the ratio between 
the sizes of the two suckers remains constant. That is, the two suckers 
grow equally evenly, although the body is growing much more rapidly 
posteriorly. 


34 ILLINOIS BIOLOGICAL MONOGRAPHS {160 


This constancy of the sucker ratio is somewhat unexpected since other 
trematodes, especially when body proportions are altered, show an increase 
of the ventral sucker over the oral. Most conspicuous is the actual reversal 
in sucker proportion in Schistosoma japonicum where, as already given, 
the ventral sucker is smaller than the oral in the cercaria, but later assumes 
equality with it, and in the adult is definitely larger. A similar tendency 
in F. hepatica has also been noted. 

The following table (Table 4, Column b/ c) shows very clearly how all 
sizes of O. cestoides vary closely about the average ratio (oral sucker .66 
of the ventral sucker). It is true that in the four smallest specimens is 
found the largest ratio (up to 0.82), but specimens almost as small show a 
ratio slightly below (0.64 and 0.65) the average, and some of the largest 
individuals show a ratio of 0.7 or more. 


TABLE 4 
SUCKER SIZE IN RELATION TO GROWTH IN O. cestoides 


Body length Body width Diameter of Diameter of 
anterior sucker ventral sucker = pis 
(a) ) () ‘ 2 
39. mm. 2.87 mm. 1.43 mm. 2.18 mm. -65 17.8 
38. 2.06 1.25 1.81 atl 21; 
38. 2.25 1.312 2s -66 19. 
32° 23 1.06 1.62 -65 19. 
Shs 3.5 1.56 2.18 71 14.2 
31. 253 133 1.8 BY 17.2 
29. Di5 1.43 2.31 -62 12.5 
29. 2:3 1; 1.56 -63 18.5 
28. 2.18 1212 5) 64 16. 
28. 123 1.37 Ze .68 14. 
28. 2AS ie 1.68 .58 16.6 
28. 2.87 1618 1.68 Wf 16.6 
26. 1.6 93 1.37 .67 18.9 
26. 1.87 1.06 1537 whe 18.9 
24.5 2.37 1525 1.87 61 13. 
24. 2.8 1.37 2.18 -62 11, 
21. oot. 1.25 175) Ae) 125 
20. 1.68 0.878 1.327 -66 15: 
19. 2.12 Ai: 1.437 71 13.9 
18. 2:5 1.14 1.77 64 10.1 
17, 225 1.028 1.77 -07 9.6 
16. 2.06 0.916 1.34 .68 11.9 
16. 255, 1.02 1253 66 10.4 
14. 1.9 1.06 1.5 : 64 9.3 
13. 2 15 175 .66 8.6 
12. 1.8 1; 1.37 .73 8.7 
1155 Pat 0.93 155 -62 7.6 
11, 1.5 0.75 1,12 .66 9.8 
6 I 2.1 0.93 155 62, Wsd 


161] SOME NORTH AMERICAN FISH TREMATODES—MANTER 35 


Tas_e 4 (continued) 


Body length Body width Diameter of Diameter of 

anterior sucker ventral sucker b c 

(a) (0) (c) c a 
10.8 mm. 1.75 mm. 0.75 mm. 1.25 mm. .6 8.6 

10.5 1.8 0.68 1.31 .52 8. 
10.5 123 0.68 1.06 64 9.9 
6.5 At 0.54 0.785 .68 8.3 

6.06 L212 0.525 0.748 ay A 8. 
3s 0.93 0.448 0.654 .67 7.6 
4.5 0.56 0.448 0.654 .67 6.9 
4.37 0.9 0.414 0.673 .62 6.5 
4.31 1.047 0.504 0.766 65 5.6 
4.18 0.937 0.467 0.635 .73 6.5 
4.125 0.991 0.397 0.617 64 6.6 
3.6 0.75 0.414 0.635 65 5.6 
2.37 0.562 0.317 0.43 Rif} 5.5 
De25 0.748 0.414 0.504 .82 4.2 

2.18 0.71 0.355 0.43 .82 5, 
1.9 0.56 0.28 0.39 74 4.8 

Average .66 


Another interesting point is the relatively much larger size of the 
suckers in comparison with body size in the young. This observation would 
follow from the fact that the diameters of the suckers keep pace with the 
width of the worm. This marked change in proportion between sucker 
diameter and body length can be followed in Table 4, column c/a. In the 
smallest specimens, the body length was 4.8 times the diameter of the 
ventral sucker, while in all the largest specimens measured the body length 
was about 20 times the diameter of the ventral sucker. The change between 
these two extremes is seen to be consistent and gradual exactly as was the 
change body length and width. Young forms in general show the body 
length to be about 5 times the diameter of the ventral sucker, medium 
sized specimens have a length about 10-11 times this diameter, while a 
specimen 38 mm. long was 21 times longer than the diameter of the ventral 
sucker. 

It is interesting to note what effect, if any, the arrival at sexual maturity 
has upon these growth rates. The uterus is located posterior to the ventral 
sucker, and it might be expected that the relatively sudden filling of the 
uterus with eggs would affect growth in this region. The body size at which 
the trematode attains sexual maturity is quite constant. Almost invariably 
eggs begin to be produced when the worm has a length of about 11 mm. 
A few eggs have been found in specimens 10.5 mm. in length. It can be 
stated quite certainly that sexual maturity is attained between the body 
lengths of 10 and 15 mm. 


36 ILLINOIS BIOLOGICAL MONOGRAPHS [162 


Reference to the charts shows 49 specimens between 5 and 10 mm. in 
length, 30 between 10 and 15 mm. in length, and 22 between 15 and 20 mm. 
in length. All specimens of these sizes were preserved. As fewer individuals 
were found intergrading between the sizes 10 and 15 mm. than between 
5 and 10 mm., it might be inferred that growth is more rapid in the former 
case. The indication can only be considered as a slight one, however, as the 
difference is not large, the numbers are somewhat few, and there is a 
possibility of various unknown factors such as infection rate. 

Further data on the effect of sexual maturity on growth can be obtained 
by comparing distances from the posterior testis to the ventral sucker 
(region of uterus) and from this same point to the posterior end of the 
worm (tail region). Ata certain period (11 to 15 mm.) the uterus becomes 
quite suddenly crowded with eggs. Whether this change alters the pro- 
portions of the length of the uterus region to the length of the posterior 
region where no organs of importance are located, and where no important 
change is occurring, can be shown approximately by comparing the lengths 
of these regions in mature and immature specimens. In 21 wholly mature 


TABLE 5 


CoMPARISON OF Uterus REGION WITH PosTERIOR Bopy REGIONS IN YOUNG SPECIMENS 
oF Otodistomum cestoides 


Body length Length of tail region Length of uterus region 

(a) (b) ae 

a 

14. mm. 6.5 mm. 5. mm a 
13. Ue 3.56 Pro 
12'. 6. 3.9 -58 
11.5 5.3 3: .56 
11), 53 3. 58 
11. 5.25 2.37 45 
10.8 5. 3525 -65 
10.5 4.8 2.87 6 
10.5 5. 2.4 -58 
10. SES 2.18 37 
6.5 3,29 1.43 44 
6.06 3: 1.47 .49 
5 233 1.12 48 
4.5 1.68 1. 6 
4,187 1.68 0.937 55 
4.37 1.5 al -66 
4.31 1.5 0.75 5 
4.125 1.9 0.687 35 
3.6 * iy | 0.57 34 
2.37 Ls 0.525 52 
2.18 0.74 0.37 5 


Average -493 


163] SOME NOR17H AMERICAN FISH TREMATODES—MANTER 37 


individuals the length of the uterus region averaged 0.67 the length of the 
tail region. In 21 immature individuals including a few very young forms, 
this uterus region averaged 0.493 the length of the posterior region. That 
is, the uterus region upon becoming filled with eggs increases on the average 
its ratio to the tail region by about 0.2. While this increase is small, it is 
very definite. Reference to Tables 5 and 6 shows that the proportion of the 


TABLE 6 


CoMPARISON OF UTERUS REGION WITH POSTERIOR Bopy REGION IN ADULT SPECIMENS OF 
Otodistomum cestoides 


Body length Length of tail region Length of uterus region b 
(a) () 
38. mm. 21. mm. 12.5 mm. 6 
38. 18. 14. a7 
32% 16. 11. 67 
31. 11.5 9. 78 
31. iy 9. .53 
29. 14. 9.75 .69 
29. 15: 8.5 .56 
28. 14. 10. will 
28. 15. 9. 6 
28. 18. Ts A 
28. 12.5 10. 8 
26. 11.06 11.06 1 
26. 15: 8. .56 
24.5 13:2 dec .53 
2h. 12.5 6.25 25 
20. 8. 8. 1 Us 
19, 10. 6.5 65 
18. het ks 5.93 ai) 
17. (aS) 5.8 .78 
16. 6.12 6.12 1. 
16. 7.9 4.6 58 
Average .67 


uterus to the tail region in the young forms measured attained only once a 
point as high as 0.7 and went as low as 0.34. Moreover, even in these forms 
the uterus region tended to be slightly greater in individuals with a few 
eggs (those specimens 10 to 14 mm. in length). Of the mature forms, 
however, the uterus region was never less than 0.4 the tail region and 
several times attained equal length with it. 

The increase of the length of the body posterior to the ventral sucker 
over the length anterior to this sucker is by no means due entirely, however, 
to this seeming increase in the uterus region. To show this fact, measure- 
ments of the neck region (that region from the anterior end to the ventral 
sucker) were compared with measurements of the tail region. The neck 


38 ILLINOIS BIOLOGICAL MONOGRAPHS (164 


region in 18 immature or recently mature forms averaged 0.77 the length 
of the tail region, while in 12 mature forms the neck region averaged only 
0.39 of the tail region. That is, while the uterus region is gaining on the 
tail region the latter is also gaining even more rapidly on the neck region 
(Tables 7 and 8). 


TABLE 7 


COMPARISON OF NECK REGION WITH POSTERIOR Bopy REGION IN YOUNG SPECIMENS OF 
Otodistomum cestoides 


Anterior end to Posterior testis to P 
Body length ventral sucker posterior end = 
(a (0) : 
13. mm. 3. mm 7. mm. 43 
11.5 335 S23 66 
11. 3. 5.3 56 
11. 3: 5.25 Ay / 
10.8 2.56 5. 751 
10.5 2.68 4.8 .56 
10.5 215 5: .55 
6.5 2.12 azo 65 
6.06 125) 3. 35) 
5: 1.87 253 81 
4.5 1.8 1.6 1.1 
4.187 1.8 1.68 1.05 
4.37 1.87 1.5 1.24 
4.31 1.37 175) 91 
4.125 1.4 1.9 74 
3.6 1.25 1.7 AY fs} 
2.3 0.93 1; 93 
2.18 - 1.04 0.74 1.4 
Average | .77 


In stating that the uterus region increases its proportion to the tail 
region, it has been assumed that the position of the posterior testis is 
relatively stationary. If, however, the uterus, in filling with eggs, pushes 
the reproductive organs backward, then the increased growth in the 
uterus region is only apparent, since the position of the hind testis was 
taken as a point of measurement. Similarly, illusions would follow from 
any local movement of the gonads either forward or backward within the 
body. In general, the gonad group appears to occupy a fixed position. 
Commonly, especially in extended specimens, the two testes are separate 
from each other by a short space. When the two organs are in contact with 
each other the surface of contact becomes flattened. Thus, if the uterus 
did have a tendency to force the gonads backward, some leeway would be 
allowed this movement before it exerted an influence on the position of the 
hind testis, upon which present measurements were based. 


165] SOME NORTH AMERICAN FISH TREMATODES—MANTER 39 


TABLE 8 


CoMPARISON OF NECK REGION witH PosTERIOR Bopy REGION IN ADULT SPECIMENS OF 
Otodistomum cestoides 


Body length Anterior end to Posterior testis to P 

ventral sucker posterior end = 

(a) (6) : 
38. mm. 5. mm. 21. mm. 24 

Sie 6. 17. <3 
38. 6. 18. 34 
29. 5 14. «35 
28. 4. 14. 28 

24.5 4, 13.2 3 

20. 4, 8. ‘5 
19. Sie) 10. =35 
18. 3. hielo .38 
ily fe 4. Ups) 53 
16. 4. 6.12 65 
16. ee) 7.9 44 
Average 39 


Some slight evidence that the crowded uterus may cause a forcing back 
of the ovary against the anterior testis is found in certain variations in 
the relative position of the pore of Laurer’s canal. This pore furnishes a 
fixed point and if it retains a constant position in relation to the ovary in 
young and in mature specimens, it can be inferred that the position of the 
ovary is also constant. Such a relation does not exist. The pore was found 
to be sometimes anterior to the anterior end of ovary, sometimes almost 
exactly dorsal to it, and sometimes slightly posterior to it. As serial sections 
were necessary to determine this point, it was ascertained in relatively few 
cases. In O. cestoides the pore was always found to be posterior to the 
anterior border of the ovary in young or recently mature specimens, and 
usually anterior to it in mature forms. One exception in both O. cestoides 
and O. veliporum shows that the pore may be posterior to the anterior edge 
of the ovary even in mature individuals. In all young forms measured the 
pore was posterior to this point. A table follows showing the position of 
the pore in specimens of different ages: 


O. cestoides 


Length Maturity . Pore in relation to Distance 
anterior end of ovary 


10 mm. uterus with few eggs Posterior 0.56mm. 
Small immature “ 0.18 
Small only a few eggs in 

uterus id 0.23 
14mm. Recently mature Anterior 0.14 
25mm. Mature 0.18 
Large Mature . 0.18 


Large Mature Posterior Slight 


40 ILLINOIS BIOLOGICAL MONOGRAPHS {166 


O. veliporum 


23 mm. Mature Anterior 0.6 mm. 


25 mm. Mature Posterior 0.285 


In any case, the extent of this shifting as far as it is indicated by relative 
pore position is not sufficient to affect materially the position of the hind 
testis. Conclusions in regard to growth changes can be more graphically 
expressed by means of a diagram (Diagram 1). 


Dracraqm. 1. Diagram to show growth changes in Olodistomum cestoides. Distance B 
constantly grows faster than Distance A, even before sexual maturity. Distance C increases 
slightly its proportion to D after sexual maturity. Distance D increases in length more 
rapidly than A, even after sexual maturity. Body length increases much more rapidly than 
body width. Size ratio of the two suckers does not change with size of the worm. Suckers are 
proportionally much larger in young. 


167] SOME NORTH AMERICAN FISH TREMATODES—MANTER 41 


COMPARISON OF OTODISTOMUM CESTOIDES AND 
O. VELIPORUM 


The close resemblance of these two species has already been noted. 
Odhner (1911b) gives the following differences: 


O. veliporum O. cestoides 

1. Size: 50 mm. by 5 to 6 mm. Size: to 65 mm. by 3 to 5 mm. 

2. Ratio of suckers: 3:5 Ratio of suckers: 3 : 4 

3. Vitellaria beginning behind the middle of Vitellaria usually beginning in front of 
uterus field, compressed into narrow middle of uterus field, not so narrowly 
bands. compressed. 

4, Egg: 0.86 by 0.06 to 0.063 mm. Egg: 0.065 to 0.072 by 0.043 mm. 

5. Thickness of egg shell 0.006 mm. Thickness of egg shell 0.003 mm. 


Of these differences, numbers 2 and 3 are certainly useless as all con- 
ditions involved were commonly found in the present studies of the single 
species, O. cestoides. Odhner placed importance on the thickness of the 
egg shell. 

Miihlschlag (1914) worked on O. veliporum and concluded that the 
following features separate it from O. cestoides: (1) its body is less in 
length, greater in width; (2) its eggs are larger, and (3) have a much thicker 
shell. He found that the thickness of the egg shell of O. veliporum to reach 
7p or more than twice as thick as commonly reported for O. cestoides. 

The trematode from Raia binoculata from the Pacific has already been 
frequently compared with O. cestoides from the Atlantic ‘‘barn-door’”’ 
skate. It has been seen that the Pacific form presents very few significant 
differences. Chief among these differences is the egg size. The average egg 
size from over 50 measurements in the Pacific form gives 85.5 by 57.8u 
as compared with 69.4 by 46.2u in O. cestoides. This difference is real, 
constant, and significant. In no case did the egg size overlap between the 
two species. Thus, the eggs in the Pacific form agree almost exactly with 
the reported egg size for O. veliporum. 

One of the other reported differences between these two species is a 
slightly greater body width in O. veliporum. The average width of 75 
Atlantic specimens (QO. cestoides) between 23 and 50 mm. in length was 
3.22 mm. The average width of 65 Pacific specimens (O. veliporum) 
between the same length limits was 3.81 mm. Thus, again the Pacific form 
agrees with descriptions of O. veliporum. The Pacific specimens were quite 
constantly of greater thickness, however, and their slightly greater width 
might be due to an average higher degree of body contraction. 

The only other specific criterion to be applied is the thickness of the 
egg shell. O. veliporum supposedly possesses a much thicker egg shell than 


42 ILLINOIS BIOLOGICAL MONOGRAPHS. [168 


does O. cestoides. In this particular, the Pacific form studied does not agree 
with the published records for O. veliporum. An average of numerous 
measurements on the egg shell gave a thickness of about 4y. For O. cestoides 
an egg shell thickness of about 4.54 was found. Thus, instead of having 
an egg shell twice as thick as does O. cestoides, the Pacific form actually 
has a slightly thinner egg shell. Measurements were taken on mature eggs 
in distal regions of the uterus. The eggs nearer the ovary had a slightly 
thicker shell. Even though this discrepancy in egg shell thickness appears 
to be a constant feature in material studied, it hardly seems to be in itself 
a specific character. In the first place, the absolute difference in egg shell 
thickness between the Atlantic form and records for O. veliporum is slight 
(about 2) since the Atlantic material showed an egg shell somewhat 
thicker than recorded for O. cestoides. Again, such minute measurements 
are difficult to determine exactly, especially as slightly oblique sections 
through the egg exaggerate the apparent thickness of its shell. Finally, 
the constanty of this feature is not well established, as is, for example, egg 
size in this genus. 

In respect to other differences noted between the two forms, the con- 
dition of the genital atrium and papilla has already been discussed and 
showed to be unreliable as a specific character. It can only be said that, in 
general, the genital papilla was either absent or small in size in O. veliporum, 
and usually prominent and robust in O. cestoides. It may, however, be 
flattened out entirely in O. cestoides and entirely protruded in O. veliporum. 

The genital organs seemed proportionally somewhat larger in O. 
veliporum. Actual measurements (in millimeters) on specimens of approx- 
imately similar size are as follows: 


O. cestoides O. veliporum 
Length Length 
32mm. | Testis (ant.) 0.9 by 0.87 32mm. | Testis (ant.) 1.25 by 1.25 
“ (post.) 1. 0.81 “ (post.) 1.5 1.25 
Ovary 0.43 0.81 Ovary 1 0.75 
31 Testis (ant.) 0.68 by 0.9 30 Testis (ant.) 1. by 0.9 
“(post.) 0.8 0.9 “ (post.) 1.27 1 
Ovary 0.5 0.68 Ovary 0.8 1 
24 Testis (ant.) 0.89 by 0.37 25 Testis (ant.) 1 by 0.89 
“ (post.) 0.78 0.86 “ (post.) 1.3 0.89 
Ovary 0.46 0.7 Ovary 0.8 0.6 


A 39 mm. specimen of O. cestoides agreed more nearly with the 32 mm. 
specimen of O. veliporum in gonad size, as follows: 
39 mm. Testis (ant.) 1.25 by 0.87 mm. 


Testis (post.) 1.37 0.9 
Ovary 0.6 0.9 


169] SOME NORTH AMERICAN FISH TREMATODES—MANTER 43 


These differences in gonad size are not, however, sufficient to be sig- 
nificant. Miss Lebour (1908) figures very large gonads for her species which 
was clearly O. cestoides. 

From this study, it has been concluded that the Pacific material repre- 
sents Otodistomum veliporum. Furthermore O. veliporum and O, cestoides 
are shown to be even more similar than has hitherto been pointed out. The 
most certain distinction is found in egg size. Raia binoculata (= R. cooperi) 
is a new host for O. veliporum. 

O. veliporum (Creplin) has the following synonyms: 


Dist. veliporum Creplin 

Dist. insigne Dies. 

Dist. microcephalum Baird } according to Ariola 1899 
Dist. scymni Risso 

Fasc. squali grisei Risso 

Dist. veliporum of Johnstone 1902 


It has been recorded from the following hosts: WNotidanus griseus, 
Notidanus cinereus, Echinorhinus spinosus, Carcharias milbertii, Raia batis, 
R. clavata, R. fullonica, R. radiata, R. lintea, R. binoculata, R. stabuliforis 
(=R. laevis), Scymnus nicaeensis, Acanthias vulgaris, Carcharias sp., 
Laemargus melanostoma, Scyllium canicula, Chimaera monstrosa, Carcharias 
rondeletti, Centrolophus pompilus. 


44 ILLINOIS BIOLOGICAL MONOGRAPHS [170 


THE MIRACIDIUM OF OTODISTOMUM CESTOIDES 
[FIGS. 31-43] 


The first larval form or miracidium of O. cestoides was studied from live 
material and in toto-mounts. As the larva is well developed and ready to 
hatch when the eggs are laid, sections of eggs in the vagina formed the 
basis for study from sections. Many thousands of the eggs can be obtained 
by cutting the adult worm just beneath the ventral sucker and pressing out 
the eggs in the distal portion of the uterus. This method gives a mixed 
culture of eggs of various degrees of maturity. A more uniformly mature 
collection results from saving only the eggs from the vagina region. Un- 
successful attempts were made to secure eggs that had been normally laid. 
Adults were kept both in sea-water and in sea-water with mucous and 
fragments from the stomach of the host. In the latter case, some specimens 
were kept alive two or three days, but in no case were any eggs obtained. 
There is no reason to believe, however, that the eggs in the vagina do not 
represent the normal condition of the eggs when laid. 

The eggs can be readily hatched. They were kept in sea-water in vials 
surrounded by running sea-water. The water in the vials was changed 
twice daily. The eggs were found to be very hardy. In mixed cultures 
containing many immature egg stages, hatching larvae appeared most 
frequently only after 7 to 10 days. In the case of cultures of only the most 
mature eggs, several miracidia were observed only 5 hours after the eggs 
had been removed from the worm. This very early hatching shows that 
the larva is fully developed in the egg at the time of oviposition. In 
general, even when the eggs in a vial seemed quite uniform, no uniform 
period of hatching was observed. Only a small proportion of the eggs 
hatched, and these hatchings, few at a time, extended over periods of some 
days (up to 15). The large number of cultures undertaken gave ample 
opportunity of studying the rather peculiar miracidium. 

The youngest immature eggs are pale yellow in color and quite trans- 
parent. They average only slightly smaller than mature eggs and the 
thickness of the shell seems to be about the same at all stages (in O. ces- 
toides). In the early stages the embryo consists of only a few cells collected 
at the opercular end of the shell, while the rest of the space is occupied by 
numerous yolk cells. These latter gradually disappear as the embryo grows, 
until the egg shell seems to contain a uniform mass of cells. 

The more mature eggs while alive have a characteristic appearance. 
The shell is brownish-yellow in color. A few small, globular bodies are 


171] SOME NORTH AMERICAN FISH TREMATODES—MANTER 45 


scattered about within the shell while at one end, the anterior, a dark 
opaque granulated area appears, concealing the anterior tip of the embryo. 
This area thins out posteriorly so that a dark crescent-shape appearance 
is given (Fig. 31). The same condition is described by Leuckart (1886:380) 
for D. lanceolatum. Just posterior to this area and within the body of the 
embryo are. two conspicuous, hump-like structures continuous anteriorly, 
but of two parts (resembling lobes) posteriorly. What was probably 
a similar structure was seen and pictured by von Nordmann (1832) for the 
eggs of D. rosaceum (= Azygia lucit). It represents a conspicuous organ of 
the embryo. Nordman noted the bifid character of the organ, describing it 
as “eine gleichsam zusammengekrummte, dunkler begrenzte Figur, welche 
an einem Ende wie mehr oder weniger gespalten ershien.’”’ All subsequent 
descriptions of the larva of A. /ucii consider the organ as simple, sac-like 
in structure and it has been interpreted as representing a simple type of 
intestine. In one case, in eggs of O. cestoides the body appeared to be split 
into three rounded lobes (Fig. 32). Even while the embryo is still in the 
egg, a more or less circular lighter area can be made out within the “‘lobes”’ 
of this organ, an appearance suggesting the presence of a lumen in each. 
The Hiillmembran of Schauinsland (1883) can be found in stained material. 
It is a thin membrane containing a few flattened cells. It is left behind 
in the egg shell at time of hatching. 

The miracidium is non-ciliated and normally pear-shaped, with a 
narrow anterior region. Its shape is continually changing, however, as the 
worm-like movement of the larva results in alternate expansion and con- 
traction of the body. When at full length the shape is narrow and elongate, 
reaching a maximum of 90 to 100u; when fully contracted the body becomes 
spherical and about 45 to 50u in diameter. The posterior end is sometimes 
pointed. The anterior end of the larva is pulled in and pushed out simul- 
taneously with the contraction and extension of the body. The action of 
this narrowed anterior region is exactly like that of a proboscis. The earliest 
movement noted within the egg can only be described as an indefinite 
“squirming.” At no time is there any indication of ciliary movement. 

The process of hatching was observed several times. At this period, 
the movement of the larva has become very definite and like that of the 
free miracidium, consisting of the alternate pulling in and pushing out of 
the somewhat pointed anterior end. The movement results in a series of 
pushes or blows directed at the operculum which sooner or later opens and 
the worm slides out. The ease of hatching seemed to vary considerably. 
Thus, one case was observed when the entire process of hatching required 
only about 30 seconds and almost without effort on the part of the embryo. 
Another case studied showed a very active embryo which did not succeed 
in hatching even after several hours and finally its movements slowed down 
and ceased. Focusing showed that this animal did not seem to be accurately 


46 ILLINOIS BIOLOGICAL MONOGRAPHS (172 


oriented in the shell and the force of the propulsion of the proboscis was 
directed a little to one side of the operculum. Although there was ample 
space for the worm to change its position, it seemed to persist in directing 
its “blows” at one spot. With the escape of the embryo from the shell, a 
small stream of minute granules is also given out. These particles attracted 
small infusorians in the culture and sometimes an empty egg shell would 
be well filled with small ciliated protozoa. 

The body of the miracidium is covered by a very thin cuticula-like 
layer which is non-ciliated. About the anterior end is a region of bristles 
or spines. Such an occurrence of spines is common in non-ciliated miracidia, 
In Azygia lucii they are described as occurring on four plates (Borsten- 
platten) surrounding the anterior end of the larva. This Azygia larva also 
has a posterior series of four bristle plates. Although Odhner (1911b) 
states that ‘‘Borstenplatten” are not present in the genus Otodistomum, 
the spiny areas were very conspicuous in living material. They were also 
discernible in toto-mounts and could occasionally be definitely made out 
in sections of embryos within the eggs. Unlike their condition in A. lucii, 
these bristles occur on five strips or areas radiating from the anterior tip. 
Each strip is tapering in form, being broadest posteriorly. The bristles are 
longer near the tip and gradually become shorter posteriorly. When the 
larva first hatches these strips or plates of bristles lie quite flat. Very soon, 
however, they become loosened at the anterior end and peel off backwards. 
This shedding of the bristle-plates often gives to the miracidium a very 
peculiar appearance, as the strips remaining attached posteriorly resemble 
appendages. The strips are of a very thin epiderm-like material, and when 
free from the larva tend to curl slightly (Figs. 34 and 43). The process of 
shedding the strips can be compared in a homely way with the peeling of a 
banana. 

Creutzburg (1890) in his work on the life history of Dist. ovocaudatum 
(=Halipegus ovocaudatus) which has a larva very much like that of 
O. cestoides, found that the miracidium of that species lost its coat of 
bristles only after it had pierced the intestinal wall of a snail. While he 
does not mention any localized areas of the bristles he describes the 
shedding of the epiderm as proceeding from the head end. He says (p. 22) 


the embryo ‘‘verwandelt er sich,....durch Abwerfen der fusseren 
stacheltragenden Bedeckung, deren Loslésung nach meinen Beobachtungen 
zunichst am Kopfpol vor sich geht..... ” Tt is therefore quite possible 


that the spiny region normally serves to aid the miracidium in piercing the 
tissues of the host. In my material, only one live individual was seen which 
seemed to have completely shed the bristle plates. 

Larvae were usually closely associated with the empty egg shell from 
which they emerged. The posterior end of the larva seemed to show a 
tendency to adhere to the egg shell. Only a few larvae were seen at any 


173] SOME NORTH AMERICAN FISH TREMATODES—MANTER 47 


great distance from their egg shells. Locomotion was certainly very limited 
and even the most active larvae progressed very little, if any, in the 
watchglasses wherein they were studied. The anterior end seemed to 
adhere rather tenaciously to any debris with which it came in contact 
(Fig. 34). 

The only conspicuous organ of the larva is the structure already 
mentioned as visible in later egg stages. It extends to about the middle of 
the body and has a paired sac-like appearance. In one favorable specimen 
it was observed that leading forward from this organ is a minute duct which 
opens at the extreme anterior tip of the larva. This anterior tip when free 
from the bristle-plates is rounded and knob-like in shape. The rounded 
lighter areas in the central part of each of the lobes of the organ have the 
appearance of lumens, and the impression gained from study of live 
material is that the entire organ represents a bi-lobed or bifid intestine. 
Such a conclusion is supported by the fact that many miracidia have been 
described as possessing a simple type of intestine. Furthermore, what is 
certainly the same structure in similar larvae (miracidia of A. lucii, 
H. ovocaudatus), has been commonly interpreted by Looss, Leuckart, 
Creutzburg, Schauinsland, and others as an intestine. 

Stained material, and especially sections through mature eggs, present 
evidence which seems to warrant questioning very seriously the conclusion 
that this organ represents any form of intestine. In the first place, the 
organ is found to consist not of two parts but of four. The outline of these 
“lobes” or parts stains with hematoxylin clearly. The bifid appearance is 
explained by the fact that the four parts are arranged in pairs (Figs. 36 
and 38). The elements of a pair are closely associated, but the pairs may 
be wide apart (Fig. 38). 

Furthermore, the central region (of each lobe) which had been inter- 
preted as a lumen, invariably stains darkly like a nucleus. The granular 
appearance of the organ in life disappears in sections and in its place is 
seen a clear transparent area. Safranin staining gave results similar to 
those obtained with various hematoxylin stains. In fact, safranin stains 
brought out the four-partite and four-nucleate condition even more clearly 
than hematoxylin. 

The fact that the organ is made up of four similar parts, and that the 
central regions stain like nuclei make it seem more probable that the organ 
is not an intestine but a group of unicellular glands. One bit of evidence in 
favor of viewing the organ as an intestine has been the reported occurrence 
of a minute pharynx or muscular region about the duct. Only the slightest 
suggestion of such a structure was detected in the present studies although 
no special staining of live material was attempted. Von Linstow (1890) 
reports what appears to be a similar structure in D. cylindraceum as a 
“Stutsapparatus.” Schauinsland (1883), however, describes and pictures 


48 ILLINOIS BIOLOGICAL MONOGRAPHS [174 


a minute pharynx-like structure in the larvae of Azygia lucit and other 
trematodes. He does not hesitate to consider such a structure as a true 
pharynx and the sac-like organ as an intestine. It is interesting to note that 
in no case does he show any form of cellular structure around the so-called 
intestine, nor does he show that any lumen is present. On the contrary, he 
does represent nuclei-like bodies within the intestine in A. /ucii larvae. 
It is quite evident that these are the same type of bodies which stain like 
nuclei in my sections. Schauinsland refers to them as ‘‘Kerne im Darmin- 
halt.”’ In one case, he reports “Im Darm bemerkt man 3 Kerne.’”’ Both 
for the larva of A. Jucii and for the larvae of the other forms he studied, 
Schauinsland shows from one to four nuclei within the contents of the 
intestine. 

Looss (1894) shows the same condition in his figures. Particularly 
interesting is his figure of the larva of A. lucit. Here three rounded bodies 
are clearly present within the organ interpreted as an intestine. In the 
present studies Azygia material was found to be most favorable in sections 
of A. acuminata. Here were found four apparent nuclei within the organ 
in question (Fig. 44). The organ seemed to be simple and sac-like in shape. 
Because of the much smaller size of the larvae in Azygia species it would 
be very difficult if not impossible to make out the four-partite condition 
which the larger larvae of Otodistomum reveal. 

The miracidium of Schistosoma japonicum possesses in addition to a 
sac-like intestine with four nuclei, a pair of large ‘‘cephalic glands,”’ one 
gland being located on each side of the intestine. The glands are nearly as 
large as the intestine. The four-partite condition found in O. cestoides 
showed, however, no such differentiation between the parts. 

Creutzburg (1890) has given not only a description of the appearance 
of this organ in the similar larva of Halipegus ovocaudatus (=D. ovocauda- 
tum), but also a history of its fate in later development. In the larva he 
studied, the organ seemed to be simple and sac-like in form. He says 
(p. 21): “Dieser kérnige Inhalt zeigt oft blischenihnliche Einschliisse, die 
auf das Vorhandensein eines Lumens schliessen lassen.’’ This larva (which 
does not hatch until the egg has been eaten by a snail) penetrates the 
intestinal wall of the snail. Soon after it has passed into the body cavity 
of the snail the larval “intestine” or organ in question begins to diminish 
in size and finally disappears. Creutzburg says (p. 21): ‘Die weitere 
Entwickelung des schlauchformigen Organs lisst sich noch bei den Sporo- 
cysten verfolgen, wo es, seine urspriingliche Lage am vordern Kérperende 
beibehaltend, spaterhin an Grésse allmihlich abnimmt, und schliesslich 
ganz verschwindet.” Creutzburg himself was somewhat uncertain as to 
the correct interpretation of the organ, but in view of its similarity to 
so-called intestines in other miracidia he concluded it represented a rudi- 
mentary intestine. 


175] SOME NORTH AMERICAN FISH TREMATODES—MANTER 49 


The conception of an intestine implies the presence of a cellular wall 
and a lumen. In none of the above instances has either of these conditions 
been demonstrated. That the organ in question might be interpreted as a 
group of uni-cellular glands seems more justified. This latter view would 
be more in accord with the nuclear-like content noted in present material 
and also described by Schauinsland and others. It would also explain the 
four-partite condition shown in Figures 36-38 and 40-41. These divisions 
of the organ into more than two parts seem to offer the strongest evidence 
against its interpretation as an intestine. Furthermore, if the possible 
glandular secretion served to aid penetration into the intermediate host, 
the gradual disappearance of the organ after this act was accomplished in 
the case of H. ovocaudatus would be explained. . The tendency showed by 
the larvae of O. cestoides to cling to debris at their anterior ends will be 
recalled. 

While it is true that the miracidia of many trematodes require no 
glandular secretion in order to penetrate their host, yet it should also be 
remembered that most miracidia are strongly ciliated and an effective 
boring force is attained by the action of the cilia which supply a constant 
forward pressure. On the other hand, the propulsive force of the miracidia- 
form under consideration is quite different in that when the force is 
directed against an object the entire body of the larva tends to be pushed 
backward. As the contents of the intestine of a snail are probabily less 
resistant than the intestinal wall, the physical power of unciliated miracidia 
would seem to be less effective in this first tissue penetration than is such 
power in ciliated miracidia. 

Unciliated miracidia of digenetic trematodes are very rare. Except 
among the Azygiidae they are definitely known only in Halipegus ovo- 
caudatus. Von Siebold as early as 1837 described an unciliated miracidium 
for Dist. variegatum (later Dist. cylindraceum=Haplometra cylindracea) 
but later workers disagreed with this conclusion. Schauinsland (1883) 
found the larva to possess a coat of cilia which it shed at time of hatching. 
Von Linstow (1890) found that the shedding of the ciliated coat was due 
to premature hatching, and that the larva is normally free-swimming. 
Willemoes-Suhm (1871) described the miracidium of Ptychogonimus 
megastomus and showed it to be very similar to Otodistomum larvae, 
possessing bristle plates and no cilia. The non-ciliated larvae of Azygia 
lucti and Halipegus ovocaudatus have been best known. Leuceruthrus now 
remains the only genus of the Azygiidae whose miracidium has not been 
studied. 


50 ILLINOIS BIOLOGICAL MONOGRAPHS [176 


NOTES ON THE LIFE HISTORY OF OTODISTOMUM 
CESTOIDES 


The very thick shell of the egg in O. cestoides indicates that these eggs 
possess the capacity for waiting a long period of time before hatching. 
On the other hand, the mature larva within the egg at the time of ovi- 
position shows that under favorable conditions the egg may hatch im- 
mediately. The further fact that the miracidium lacks the power of 
locomotion indicates that the eggs do not normally hatch until eaten by 
a snail. Schauinsland (1883) believes that such is normally the case for 
Azygia lucii, the eggs of which he found hatching in the intestine of a snail. 
Leuckart (1886:66-67) says that this condition is probably true for all 
unciliated miracidia. He states: “unter den Arten mit glatter Embryonal- 
haut scheint es doch manche zu geben, die im Wasser entweder gar nicht 
oder doch nur selten ausschliipfen, vielmehr solches vermuthlich erst dann 
thun, wenn sie, noch umschlossen von der Eischale, in den Darm eines 
geeigneten Trigers gerathen sind. So sah ich die Embryonen des Distomum 
ovocaudatum niemals im Freien ausschliipfen, obwohl ich die schon im 
Mutterleibe vollstindig sich entwickelnden Eier wochenlang, bis zum 
Absterben, im Wasser cultivirte. Eine ahnliche Beobachtung machte 
Schauinsland an Dist. tereticolle, dessen Embryonen im Darme von Lymna- 
eus palustris und L. stagnalis noch nach 24-36 Stunden lebhaft umher- 
kriechen, aber im Wasser nur selten frei werden.” 

The larvae of Halipegus ovocaudatus after hatching in the intestine of 
the intermediate snail host develop into sporocysts as shown by Leuckart 
and Creutzburg. The explanation of the ready hatching of the eggs of 
O. cestoides in sea water is found in the effect of the changes in concentration 
of the sea water due to evaporation. This effect’ was accidentally dis- 
covered when a culture of mixed eggs was left exposed in a watch glass for 
several hours. Evaporation of the sea water caused the opercula of the 
eggs to open whereupon the larvae, even though immature, partially 
escaped. The same result was repeatedly noted when sea water containing 
eggs was allowed to evaporate. The more mature eggs hatch more readily 
and the larvae appear active and healthy. When the evaporation is pro- 
nounced the less mature eggs open and the embryos partially slide out 
from the shell. Embryos thus prematurely hatched show no movement. 
Young eggs wherein the body form of the embryo is not definitely estab- 
lished do not open. In regular cultures the evaporation was slight and 
gradual, so that only mature eggs were stimulated to hatch. . 


177] SOME NORTH AMERICAN FISH TREMATODES—MANTER 51 


Still further evidence that the eggs do not normally hatch in a free 
state is furnished by the following data: Three vials of fresh eggs were 
covered with an animal parchment membrane and immersed in a large 
aquarium of running sea water. Here any change of concentration due to 
evaporation would be negligible. Although all of these cultures were 
examined at intervals for about a week, no hatched eggs or larvae were 
found, while eggs collected at the same time but kept in open vials hatched 
with customary regularity. This experiment to eliminate evaporation was 
tried with the purpose and hope of increasing the hatching of the eggs. 
The fact, however, that this more normal environment of the eggs reduced 
or eliminated hatching is in full accordance with the later discovered cause 
of hatchings by evaporation of the sea water. 

The opening of the operculum of the egg shell therefore seems to be 
induced directly or indirectly by an increase in density or osmotic pressure 
in the surrounding medium. The indication is that the stimulus is primarily 
a physical one rather than a chemical one. That is, increased density in 
the content of the snail’s intestine as compared with the density of sea 
water, rather than any chemical peculiarity of the location within the 
snail, induces the hatching of the eggs. This conclusion receives support 
from Schauinsland’s experiments in hatching the eggs of A. lucii. He 
obtained normally laid eggs, and found that the speed of their hatching 
could be greatly increased by placing them in a solution of common salt. 
In this solution the eggs hatched in about 15 minutes or practically im- 
mediately. It seems clear that no particular chemical substance is necessary 
for the stimulation to hatch, but merely an increase in osmotic pressure in 
the surrounding medium. Whether such a stimulus to hatch is direct or 
indirect is, of course, unknown. It is possible that the discrepancy in 
densities within and without the egg shell stimulates a secretion from the 
gland cells of the embryo, and that this secretion is the direct cause of the 
opening of the operculum. Some evidence in favor of this possibility is 
seen in the fact that even excessive evaporation does not cause the younger 
eggs to open although the operculum is well defined in the one-celled egg 
stage. 

Various molluscs common in the vicinity of Frenchman’s Bay were 
kept in vials of egg cultures. After periods varying from about 12 hours up 
to several days, these molluscs were removed and examined microscopically 
by means of smears. In general, all of this work was unsatisfactory. Eggs 
retained between the shell and body of a snail showed a tendency to hatch 
after the snail had been out of water for some time. This result would be 
expected, being probably due to sea water evaporation. There was no 
evidence that larvae so hatched penetrated the tissues of the snail. Un- 
fortunately, during most of the work, no special examination was made 
for the presence of eggs in the intestine. One very conspicuous case was 


ILLINOIS BIOLOGICAL MONOGRAPHS {178 


on 
to 


discovered, however, when it was found that Littorina litorea ate these 
eggs very readily. Pellets of fecal or food matter in the intestine showed 
eggs present in large numbers. The snail had been kept for four days in a 
vial containing eggs. One pellet from the intestine contained over 50 eggs, 
another 25, 15, 12, etc., down to 4 or 5. A live larva was found by lightly 
crushing one of these pellets under a cover glass. The location and con- 
dition of this larva leaves no doubt that it had recently hatched from one 
of the eggs in the intestine of the snail. The snail had been dry and out of 
water for about a day and a half. Two out of six other specimens of 
Littorina examined by smears showed eggs in the intestine. This condition 
was further investigated by examination of serial sections of snails exposed 
to eggs. All of four specimens of Littorina so sectioned showed numerous 
eggs in the intestine. These eggs sometimes occurred in large numbers 
(several hundred). One case of a partly hatched larva was discovered in 
these sections. Careful examination revealed no certain case wherein such 
Jarvae had penetrated the wall of the intestine. Serial sections of two 
specimens of Thais lapillus, one of which had been in a very vigorous 
culture for over a week, gave practically negative results. Occasionally, 
isolated eggs were found in the digestive tract of one of these specimens, 
while the other contained no eggs. Sections of Buccinum undatum (which 
had, however, been in the egg culture only one night) showed no eggs. 

An encysted distome was not uncommon in both Littorina and Thais, 
but it could not be determined as Otodistomum. It occurred in thin walled 
cysts near the digestive tract. Redia and cercaria were also found in these 
snails, but probably those discovered did not belong to Otodistomum. 
No definite conclusions can therefore be drawn in regard to the first inter- 
mediate host, except that some species of snails (especially Littorina) 
readily devour the trematode eggs, and that these eggs can hatch in the 
intestine of the snail. Other species of snails under similar conditions seem 
to eat very few or none of the eggs. 

In the meantime, rather conclusive evidence has been found in regard 
to the last intermediate host of this trematode, at least in European waters. 
Scott (1909), in his report on fish parasites of Scotland waters, states in 
his discussion of Dist. cestoides: ‘“‘Several young specimens of a Distomum, 
which closely resembles the immature D. cestoides from the skate, were 
found encysted on the walls of the stomach of a Witch Sole, Pleuronectes 
microcephalus, captured in Moray Firth. There were several cysts observed, 
and all those examined contained only young Distomids—in some cases 
one, in others two examples. 

“Fishes form a considerable proportion of the food of large skates, and 
probably the Witch Sole, which lives in moderately deep water, sometimes 
becomes the prey of these large Plagiostomes.” 


179] SOME NORTH AMERICAN FISH TREMATODES—MANTER 53 


Nicoll (1913a) records Otodistomum cestoides (van Ben.) from Raia 
macrorhynca and adds the following: “In regard to the life history of this 
species, it is probable that the cercaria discovered by Scott, encysted in 
the stomach wall of the witch, Plewronectes cynoglossus (in Scott’s paper 
this species is inadvertently named P. microcephalus) represents the larva 
of O. cestoides. In the same fish I have found encysted in the wall of the 
stomach a cercaria, which from its large size and general structure, cannot 
be referred to any other species. It occurred as a large orange-yellow 
globular cyst 1.95 mm. in diameter, firmly attached to the outer wall of 
the stomach by a short pedicle. The wall of the cyst consisted of a thick, 
tough outer coat within which was a large amount of viscous yellow 
material. The cercaria measured 2.4 mm. in length, with a maximum 
breadth across the ventral sucker of 0.66 mm. Both suckers were trans- 
versely elongated, the oral measuring 0.29 by 0.35 mm. and the ventral 
0.43 by 0.59 mm. The latter was situated at a distance of 0.96 mm. from 
the anterior end. The pharynx was small and situated close to the oral 
sucker. There was a very short esophagus and wide diverticula extending 
in a slightly sinuous manner to the posterior end of the body. The excretory 
vesicle was Y-shaped and consisted of a median stem extending a quarter 
of the length of the body, and two lateral branches reaching forward as 
far as the pharynx. No other organs were visible.” 

This cercaria described by Nicoll resembles almost exactly my youngest 
forms from the skate. A copy of Nicoll’s figure is given for comparison 
(Figures 2 and 3). As Nicoll points out, no other trematode is known to 
which this cercaria could belong except O. cestoides. Reference to my 
records shows that the sand dab and flounder are among the most common 
fish food of the big skate. No cysts were found containing cercaria, but 
relatively few of these flat fish were examined. It is very probable that the 
sand dab or flounder conveys the trematode to the big skate. The degree of 
infection and range of size of the parasite in the skate indicating a con- 
tinuous infection is in accordance with this conclusion. 

The immature trematode found encysted in the stomach wall of Lophius 
piscatorius and named ‘‘Xenodistomum melanocystis” by Stafford appears 
to be an immature O. cestoides. It is so identified by Odhner (1911b), who 
concludes that the goose-fish does not represent a true intermediate host, 
but that the cysts in that host represent an accidental infection. 


54 ILLINOIS BIOLOGICAL MONOGRAPHS [180 


SYSTEMATIC REVIEW OF THE FAMILY AZYGIIDAE 


The characteristics of the family Azygiidae as given by Odhner (1911b: 
513-14) are as follows: 


Mehr oder weniger langgestreckte und abgeplattete “‘Distomen” mit einem derben, 
muskelkriftigen Kérper von 5-75 mm. Linge. Saugnipfe sehr kriftig entwickelt, einander 
genihert. Haut unbewaffnet, mit dicker Cuticula, die sich beider Kontraktion in unregel- 
missige Querfalten legt. Darm mit kriftigem Pharynx, dusserst kurzem Oesophagus 
und bis ins Hinterende reichenden Darmschenkeln; ein Pripharynx fehlt. Excretionsblase 
Y-férmig mit sehr langen, bis ins Kopfende reichenden (und sich dort mitunter vor dem 
Mundsaugnapf vereinigenden) Schenkeln. (Bei Ptychogonimus ist der Hauptstamm sehr 
verkurzt.) Genitalporus median, zwischen den Saugnipfen. Die charakteristische Ent- 
wicklung der Endteile der Geschlechtsweg biétet die beste Biirgschaft fiir die nahe Ver- 
wandtschaft der in diese Familie zusammengestellen Gattungen: der Genitalsinus ist sehr 
geriumig entwickelt; die minnlichen Leitungsweg bestehen aus Ductus ejaculatorius, Pars 
prostatica und Samenblase, die beiden letzteren schlauchférmig und ausser bei Ptychogonimus 
von einem Cirrusbeutel umhiillt; die ganze Komplex liegt unmittelbar vor oder iiber dem 
Bauchsaugnapf. Ovar und Hoden median, unmittelbar hintereinander in Hinterkérper 
gelegen. (Ausnahme: Leuceruthrus.) Uterus von Ovar aus nach vorn ziehend (Da er bei 
Ptychogonimus vor dem Ovar zuwenig Platz fiir seine Entfaltung findet, sendet er jederseits 
zwischen den Geschlechtsdriisen und Dotterstécken eine lange Schlinge nach hinten bis in 
die Nihe des Hinterendes). Laurerscher Kanal vorhanden, Receptaculum seminis fehlt. 
Dottersticke follikulir entwickelt, in den Seiten des Hinterkérpers, nicht bis ins dusserste 
Hinterende reichend. Vagina vorhanden. Fier etwa 0.045-0.085 mm. lang, gedeckelt; sie 
enthalten bei der Ablage ein reifes, anscheinend immer unbewimpertes Miracidium.— 
Magenparasiten bei Fischen. 


Odhner included the following genera in this family: Otodistomum, 
Azygia, Leuceruthrus, and Ptychogonimus. Azygia and Otodistomum are 
the most nearly related genera. Leuceruthrus has a very different arrange- 
ment of gonads, and Goldberger (1911:7) suggested that it might represent 
the type of a new family. In this genus the testes are lateral and anterior, 
being far removed from the median and more posterior ovary. Odhner, 
however, shows that this forward migration of the testes is of secondary 
importance, compared with the similarity which the genus shows to Azygia 
in the character of the genital atrium. Ptychogonimus shows the most 
marked deviations from the family type. These deviations lead toward 
certain characteristics of another group of marine trematodes known as 
the Distomum-clavatum group. Consideration of this relationship might 
be of value in determining the systematic position of the family Azygiidae. 

Trematodes of the Dist. clavatum group are also of large size with 
powerful, muscular bodies, and are found in the stomachs of marine fish. 
The group, containing a number of species, has been an isolated one 


181] SOME NORTH AMERICAN FISH TREMATODES—MANTER 55 


taxonomically. In 1911, Odhner placed the group as a sub-family of the 
Hemiuridae. Although designating these forms as of sub-family rank, he 
did not give a sub-family name. Nicoll (1915) in his list of trematodes of 
British fish, classified them under the Accacoeliinae. The term “Dist. 
clavatum group,” although awkward, is curiously persistent. The species 
in question (Dist. clavata (Menz.) Rud.) is actually Hirudinella clavata as 
designated by Blainville in 1824. Blainville later included also in this 
genus the former Fasciola ventricosa. The forms have been usually referred 
to the genus Distomum. All species in the group probably belong to the 
genus Hirudinella. 

Similarities of this group to the Azygiidae in general are: large size, 
muscular bodies, no pre-pharynx, very short esophagus, similar excretory 
system, and similar genital atrium. This latter condition forms a very 
important and striking resemblance. Jigerskiold (1900) describes the 
genital sucker of Distomum megastomum (= Ptychogonimus megastomus) 
as “ein neuer Typus von Kopulationsorgenen.’’ He compares the terminal 
genital regions of D. veliporum, D. clavatum, D. verrucosum, and D. megasto- 
mum, and offers the suggestion that the latter (which now represents the 
genus Ptychogonimus) is phylogenetically derived from a form resembling 
D. veliporum through a series now represented by members of the Dist. 
clavatum group. ‘This suggestion is based solely on comparison of the 
“Kopulationsorganen.’”’ The comparison does show that so far as the distal 
genital apparatus is concerned, Ptychogonimus is more similar to the 
Hirudinella group than to the genera of the Azygiidae. This similarity is 
marked not only by the more conspicuous folds and muscle rings in the 
wall of the atrium, but also by the fact that both sex ducts open separately 
on the genital papilla in Ptychogonimus and in Hirudinella. 

The lack of a cirrus sac in Ptychogonimus is another important feature 
in which that genus is like Hirudinella and different from other Azygiidae. 
Furthermore, the uterus in Ptychogonimus sends two coils posterior to the 
ovary and extending nearly to the posterior end of the body. This dis- 
tribution of the uterus is unlike anything found in other Azygiidae but 
very similar to the condition in Hirudinella. 

Odhner’s distinction between the Azygiidae and the Hirudinella group 
is that in the latter not only have the testes migrated forward (as in 
Leucerthrus) but the ovary has followed also. The ovary is then located 
directly behind the testes instead of in front of them as is the normal 
condition in the Azygiidae. He continues (p. 524): ‘‘—dadurch werden 
also die Lagebeziehungen zwischen Ovar und der Hauptmasse des Uterus 
die umgekehrten zu denen der Azygiiden. Nach diesem zweifellos recht 
schwerwiegenden Merkmal habe ich in erster Linie die Familiengrenze 
gezogen.” 


56 ILLINOIS BIOLOGICAL MONOGRAPHS [182 


However, as two coils of the uterus extend posteriad in Ptychogonimus, 
in this genus also the chief mass of the uterus is posterior to the ovary as 
can readily be seen from the figures of Jacoby (1899). One of the chief 
distinctions, then, between this genus and the Hirudinella group seems to 
be the position of the ovary in relation to the testes. Yet the significance 
of gonad location was discounted by Odhner himself when he included 
Leuceruthrus in the Azygiidae. Ptychogonimus, however, possesses 
follicular vitellaria as in Azygia, and not tubular as in Hirudinella. Again, 
its body is flattened and less muscular than Hirudinella. Considering these 
latter features, the genus is probably more appropriately considered as a 
member of the Azygiidae. Yet evidently it shows a relationship between 
the two groups and through it the family Azygiidae leads to the Hemiuridae 
and to a sub-family near the Accacoeliinae. 

The miracidium of Ptychogonimus is non-ciliated and bears a spiny 
anterior region as does the miracidium of Azygia. Odhner considers 
Ptychogonimus to be more closely related to Azygia than to Otodistomum 
“namentlich auf Grund des Baues der Miracidien.” It has, however, 
already been shown that Otodistomum larvae are also equipped with 
bristle-plates. This inference of relationship between genera on the basis 
of larval forms is interesting. No description of the miracidia of Hirudinella 
species could be found, but, judging from sectioned material of Hirudinella 
fusca, the mature eggs in this species do not contain larvae at all similar 
to those contained in mature eggs of Otodistomum. Hence, the first larval 
form of Ptychogonimus probably relates that genus more closely to the 
Azygiidae than to Hirudinella, 7f similarity of larval forms is reliable 
evidence. But there is reason to believe that similarity in miracidia of 
different species does not necessarily indicate close specific or even generic 
relationship of the adult trematodes. Thus, the miracidium of Halipegius 
ovocaudatus, a parasite of the frog, has the very same morphological 
features that characterize the miracidia of Azygia and Otodistomum. It is 
of the same shape and movement, is unciliated, possesses bristle plates, 
and has the so-called “intestine” (Creutzberg, 1890). Yet the adult form 
of Halipegus is not closely related to Azygia. The natural explanation is 
that the adults have undergone evolution independently of their larval 
forms. The non-ciliated miracidium is probably always associated with 
the fact that the egg normally hatches only after eaten by a snail. The 
retention of this feature in developmental history results in the retention 
of a certain type of larva. In the meantime, the adults (in the two cases 
cited) seem to have evolved along different lines without change in their 
miracidia. That is, one finds here the very common condition of constancy 
of larval forms and divergence of adults. The other possibility of con- 
vergence of larval forms is not probable in this case because the miracidia 
resemble each other in such great detail. 


183] SOME NORTH AMERICAN FISH TREMATODES—MANTER 57 


The genera of the Azygiidae can be separated by the following key: 


Uterus sending coils posterior to ovary................-.0005 Ptychogonimus 
Uterus entirely anterior to ovary 
Ovary and testes more or less directly behind one another in 
median line 
Genital pore close to acetabulum, branches of excretory 


SYSLEMUSEPATALG aaa ace cereieul esa eis teicieme re sdiete tiaceue ine ... Azygia 
Genital pore nearer oral sucker, branches of excretory 
vesicle united anterior to oralsucker............ Otodistomum 
Testes lateral and anterior to ovary.............00 0000 eee cece Leuceruthrus 


Ptychogonimus has the single species megastomus. Leuceruthrus micro pteri 
is the only representative of the genus Leuceruthrus. 

The two species of Otodistomum have already been considered at 
length. The egg size is the most certain distinction between them. 


Eggs averaging about 69 by 46u................ ......0. cestotdes 
Eggs averaging about 86 by 58u................-..055 O. veliporum 


A key to the species of Azygia will follow later. 

Azygia is the only genus of the family showing taxonomic confusion in 
its species. As it is morphologically very similar to Otodistomum, some 
of the difficulties leading to confusion were encountered in the present 
studies, and led to further comparative study of different species of Azygia 
as well as of the two genera themselves. These difficulties involved the 
question of relative significance of such factors as: body size and shape; 
extent and arrangement of the vitellaria; relative size and position of the 
suckers; shape of pharynx; position of gonads; and size of eggs. 

In the first place it is important to note that these forms are all very 
muscular and highly contractile. Their nature in this respect can be 
contrasted with such forms as Dicrocoelium and Opisthorchis, so that 
even though the internal arrangement of organs may,be similar, the heavy 
muscular body sharply distinguishes the Azygia group from them. Looss 
noted this fact in 1899 when he pointed out that the common descriptions 
of A. lucii (= Dist. tereticolle) hardly separated it from the genus Opis- 
thorchis. Yet Opisthorchis is a delicate, quite muscularless form, and not 
closely related to Azygia. 

Body contraction in the Azygia group where the worms are elongate in 
form not only alters the general shape, but it also changes the relation of 
the ovary and testes so that the former may lie almost lateral to the 
anterior testis, instead of directly anterior to it. In spite of the fact that 
Goldberger (1911) noted this variation in his A. acuminata, he nevertheless 
separated his genus “‘Hassalius’’upon this condition. The genus Hassalius 
has already been rightly reduced to synonymy with Azygia by Odhner 
(1911b) and by Ward (1917). Moreover, body contraction results in 
throwing the intestinal ceca into folds, giving them a zig-zag appearance. 


58 ILLINOIS BIOLOGICAL MONOGRAPHS [184 


Such an appearance is entirely without significance except as it indicates 
to some extent the degree of contraction. It should be eliminated as 
a distinction between species. A pointed or blunt caudal region is also a 
character depending largely upon temporary body contraction. 

Some confusion among genera and species is also due to a rather extreme 
range in size exhibited by the trematodes of this group. The conspicuous 
growth of Otodistomum cestoides even after arrival at sexual maturity, has 
already been considered. While this feature is common among trematodes, 
it seems to be particularly prominent in Azygia species. Odhner is therefore 
justified in considering Stafford’s genera, Megadistomum and Mimo- 
distomum (which were largely based on body size) as synonymous with 
Azygia. ; 

The extent and arrangement of the vitellaria are often very constant in 
trematodes. In the Azygiidae, the vitellaria are less reliable for specific 
diagnosis than might be expected. The variability of these organs in 
O. cestoides has been noted in detail. Odhner allows them almost unlimited 
range in Azygia species also. Certainly the importance given to details of 
these organs by Goldberger has been unwarranted. In the present studies, 
the constancy of the vitellaria in the various forms was critically studied, 
and will be considered in connection with the different species. 

One histological feature of special interest in highly muscular trema- 
todes such as the Azygiidae, is the arrangement of body muscles. Body 
muscles in trematodes usually consist of certain layers (circular, longi- 
tudinal, and diagonal) immediately beneath the cuticula. In addition to 
these muscle layers of the body wall, there occurs in the present group a 
well developed layer of longitudinal muscles within the parenchyma. 
These muscles running parallel with the longitudinal muscles of the body 
wall occur in bundles forming a more or less compact layer, so that in 
cross-section there is separated a central region containing most of the 
organs from an outer cortical region. Ward (1910) called particular 
attention to these muscles in Azygia sebago. They were also described and 
figured by Leuckart (1886) for Azygia tereticolle. Concerning them Leuckart 
(p. 18-19) says: ‘‘Unterhalb des Hautmuskelschlauches ordnen sich diese 
Parenchymfasern hier und da wieder in formliche Schichten, wie z.B. bei 
Distomum tereticolle, bei dem sich in einiger Entfernung von den Diagonal- 
muskeln der Rinde eine scharf begrenzte zweite Lingsfaserschicht bildet, 
die aus kriftigen Spindelzellen besteht und mit Ausschluss der Dotterstécke 
die in dem hellen, von Bindegewebe erfiillten Zwischenraum zwischen ihr 
und dem Hautmuskelschlauche zu liegen kommen, simmtliche Eingeweide 
in sich einschliesst.’’ Thus, the vitellaria occurred outside the muscles, as 
Ward found for A. sebago. In the present study of different American forms 
of Azygia, the vitellaria always occurred outside this muscle layer. The 


185] SOME NORTH AMERICAN FISH TREMATODES—MANTER 59 


available sections of Goldberger’s A. acuminata showed the muscles less 
developed and more widely scattered. 

The occurrence of similar body muscles in Otodistomum serves as an 
additional histological link of relationship between these forms and Azygia. 
Villot (1879:7) describes the grouping of such muscles for D. insigne 
(=Otodistomum veliporum). Ue says: ‘Une derniére couche de fibres 
longitudinales disséminées dans la zone limite du parenchyme. Ces fibres 
sont trés-fortes.’’ Villot’s figures clearly show these muscles as a definite 
layer. They represent a condition similar to that found in Azygia species, 
but their position is distinctly different in Otodistomum where they com- 
pletely enclose the vitellaria. My own studies on Ofodistomum cestoides 
and O. veliporum show the muscles present in a discernible layer but more 
scattered than in Azygia species, and external to the vitellaria. 

What may represent a homologous arrangement of longitudinal muscles 
has also been described for trematodes of the Hirudinella clavata (= Disto- 
mum clavatum) group. These forms are extremely muscular and contractile. 
In the neck region of H. clavata the following muscle layers occur: circular 
layer, longitudinal layer, oblique layer, and finally another internal zone 
of longitudinal muscles. Concerning this latter, Poirier (1885:483) says: 
“Celle-ci se compose d’un grand nombre de faisceaux musculairessouvent 
trés gros, et formés de fibres longitudinales d’un fort diamétre.” Poirier 
describes a rather peculiar condition posterior to the ventral sucker. In 
this region, he says (p. 484): ‘‘toutes les zones de fibres musculaires a 
Vexception de celle des faisceaux longitudinaux internes, ont complétement 
disparu. Cette derniére, par contre, a pris un développement considérable. 
Elle est formée de faisceaux composés d’un grand nombre de fibres, trés 
serrés les uns contre les autres, de facon 4 former une gaine épaisse, 4 peu 
prés continue, 4 lantérieur de laquelle se trouvent le parenchyme du corps 
et les différents organs de l’animal.”’ 

I have found (in agreement with Miihlschlag, 1914) a similar condition 
in Hirudinella fusca. The other body muscles, however, do not here com- 
pletely disappear as recorded by Poirier. Throughout the body length in 
this form there occur from the cuticula inward the following muscle layers: 
(1) circular, (2) longitudinal, (3) circular, (4) longitudinal. Layer (2) is 
always very weak with only scattered fibers. In mid-body region, layer (4) 
is very powerful with heavy fibers grouped in large bundles. It is this inner 
layer which is possibly homologous with the internal parenchyma muscles 
of Azygia and Otodistomum. It differs from them in being immediately 
surrounded externally by a ring of circular muscles. Granting that these 
muscles are present in all three groups, they differ in Azygia species by 
being located internal to the vitellaria, whereas in Otodistomum and 
Hirudinella they are found external to the vitellaria. 


60 ILLINOIS BIOLOGICAL MONOGRAPHS [186 


The writer has been fortunate in obtaining for study type or original 
material of all the different Azygia forms described from America with the 
exception of those recorded by Stafford. Co-type material of Azygia 
perryit Fujita from Japan was also studied. The conclusions reached will 
be included under the following discussions of accepted species. 


AZYGIA ANGUSTICAUDA! (STAFFORD 1904) 
[Fig. 27] 


Synonyms: Mimodistomum angusticaudum Stafford 1904 
Azygia loossii Marshall and Gilbert 1905 
Azygia loossi Odhner 1911 


The descriptions of the two above mentioned forms appeared at about 
the same time. Since in the present work material was obtained only of 
A. loossii, the distinctive specific characters will be taken from that 
material. Goldberger (1911) has redescribed this species at some length. 
Reference to Stafford’s description will be made a little later. 

The position of the gonads in the extreme posterior region of the body 
seems to be a point in which A. Joossii is distinct from all other species. 
In this form the testes are located about 1/7 to 1/8 the body length from 
the posterior tip. Furthermore, the ventral sucker in this species is only 
slightly anterior to the middle of the body, whereas in other species it is 
distinctly more anterior. Such marked differences could possibly be 
explained by a highly extended anterior region and a highly contracted 
posterior region. But in the few specimens available, it was very clear that 
the entire body was extended. The uterus in A. loossii appears to be tubular 
with eggs in linear order, but this condition may be due to the possibility 
that the specimen had but recently arrived at sexual maturity. The 
musculature of the genital atrium seems to be particularly well developed 
in this species, so that the genital pore appears to be surrounded by a small 
sucker. The eggs average about 52 by 28y which is intermediate between 
the recorded sizes of eggs in A. sebago and A. acuminata. 

What seems to be an additional important feature of this species is 
the extent of the vitellaria almost to the region of the ventral sucker. 
Although the vitellaria actually begin in the mid-body region instead of 
anterior to it as is common in other species, the fact that the ventral 
sucker itself is equatorial in position explains the relative proximity of the 
vitellaria to it. The proportion of body length to distance from ventral 
sucker to most anterior vitellaria was found to be 27.2 and 26.2, a ratio 
reached only by A. acuminata. (See Table 18.) A. loossii was collected 


1 Due to an obvious misprint the name of this species was spelled “augusticaudum” 
in Stafford’s original paper. 


187] SOME NORTH AMERICAN FISH TREMATODES—MANTER 61 


from Micropterus salmoides, Lucius lucius, and Amia calva from Wisconsin 
lakes. 

The above characters do not seem to warrant a new genus for this 
species, as in every important respect it agrees with the genus Azygia. 
It seems quite certain, however, that it does represent the same form 
described by Stafford as ““Mimodistomum augusticaudum’” from the mouth, 
pharynx, esophagus, and stomach of Lota maculosa and Stizostedion 
vitreum. Stafford describes the ventral sucker ‘‘as situated in the middle 
of the length of the worm in the most normal cases. The genital glands 
are flattened against each other and crowded backwards near to the ends 
of the caeca.”” Comparing it with Azygia, he says: “In the 12 mm. Azygia 
I selected as example, the ventral sucker is 2 mm. from the anterior end. 
In the 7 mm. Mimodistomum it is 3.5 mm. from the end, while the relatively 
long distance between sucker and ovary is in marked contrast to the short 
distance between the latter and the posterior end of the worm.” 

Thus, although Stafford’s description is brief, the differences he points 
out are exactly those between A. Joossii and other American species. That 
is, there is no point in Stafford’s description of ‘‘Mimodistomum angusti- 
caudatum”’ that does not agree with A. Joossii and practically every point 
mentioned is characteristic for that species. Hf, therefore, Stafford’s 
description is to be accepted there seems to be no escape from considering 
the two species synonymous. 


AZYGIA ACUMINATA GOLDBERGER 1911 
[Figs. 21, 22] 


Goldberger unfortunately emphasizes unimportant points (e.g., vitel- 
laria unbroken, ceca zigzag, tail pointed, constricted neck region) in 
distinguishing this species. A study of his material, together with specimens 
of the same species collected and identified by Cooper, has led to the belief 
that this form represents a true species capable of distinction by definite 
features. A few specimens* from Dr. Ward’s collection from the same host 
(Amiatus calvus) apparently also belong to this species. 

Certain similarities in all of the material could be demonstrated. The 
constriction of the neck just anterior to the ventral sucker appears to be 
fairly constant and noticeable. This character should not be emphasized, 
however, as Goldberger’s own figure of his Azygia bulbosa shows that 
some slight localized and temporary constriction may occur in this region 
in other species. The most distinguishing specific characters were found 
to be: relatively wide body, anterior extent of the vitellaria, egg size, and 
poorly developed condition of the internal parenchyma muscles. It should 
be realized that the nature of all of these features is of somewhat precarious 


* Collection of Dr. H. B. Ward, vials Nos, 25.27 and 25.28. 


62 ILLINOIS BIOLOGICAL MONOGRAPHS [188 


standing in this genus. Probably no one of them, unless very marked, 
would justify a recognition of a separate species. Only because of the 
general association of all of these characters can the forms be separated 
from the other common American species. It may also be of some sig- 
nificance that all of the material is from the same host, Amiatus calvus. 

The proportion of body width to body length can be seen in Table 15. 
This point cannot be considered a reliable specific character. Generally 
speaking, A. acuminata usually shows a wider body than most of the other 
forms. 

In nearly every case, the vitellaria began at about the level of the 
posterior edge of the ventral sucker, rarely appreciably posterior to it. 
In none of the other American species was this general condition found 
except in A. angusticauda (Staff.) wherein this matter has already been 
discussed. Table 18 compares A. acuminata with the other forms in this 
respect. 

The average egg size of twenty measurements from Cooper’s specimens 
was 64.8 by 28u. The average egg size of about fifty measurements from 
Goldberger’s specimens was 63.4 by 34u. The egg size in Ward’s material 
was 63 by 29u. All of these averages are considerably above the egg size 
of the most nearly related Azygia species (Table 14). This large size is 
attained in the largest specimens of a few forms (like Leidy’s Dist. longum), 
but was never found in specimens of sizes similar to A. acuminata. 

Four sectioned specimens (three from Goldberger’s material, and one 
from Cooper’s) agreed in showing a much more scattered and less compact 


TABLE 9. Asygia acuminata 
Measurements in millimeters 


gfele? lee. | 28 | 32 | 23 
5 Za »|BelBos/ Ba ESse] BS2 lag] ag 
bo S| aed |e AS seas i elas ol mete o§ SES 
8 Me) a3 aS gad Pn eC 2h a sp 
4H S&S |/Oo8g/>2 [ae 8)a 5 sass as SS O60 |\\ieea 
8.* 1.68: | 1. 0.75 2.6 343 0.4 1.37 0.31 0.31, 
11.3* 225 133 1. 3.9 0.65 2.56 1.56 0.96 
10.9* 2:5 £3 0.93 3.4 3.87 0.37 2t5 0.63 1.01 
O275* | 153 iI 0.68 3.3 3.1 0.5 2.4 0.5 1.5 
e285 1255/18 3.87 0.74 
968% [2255 1S 1. 3 3.75 0.3 
9.87* | 2.6 1.25 | 1.06 3.56 3.62 0.35 1.4 0.65 1.15 
6.87 1.8 1.18 | 0.9 1.9 200 0. 1.6 0.78 0.84 
6.56 1.75 | 1.06 | 0.74 223 1.75 0.5 156 0.95 0.76 
6.3 135 0.93 | 0.78 2. 2.18 0. 1.4 0.84 0.13 
a5 2° 1.18 | 1. 2.68 2375 0. 1.68 0.88 1.03 
8.877 | 1.4 0.87 | 0.812 2.93 Rigs) 0:3 2218 1.5 1.56 
9.377.) 1:3 0.87 | 0.812 3.75 320 0.75 2.18 0.87 1.18 
1 oF 0.93 | 0.75 3.87 4.12 0.5 2.8 1.87 1.9 


189] SOME NORTH AMERICAN FISH TREMATODES—MANTER 63 


arrangement of internal, longitudinal parenchyma muscles than was found 
in the other Azygia species. 

Table 9 (page 60) gives measurements of the available A. acuminata 
specimens. Those marked * were collected by Cooper; those marked + 
are from the Ward collection and were obtained at Fairport, Iowa, in 
1916 by T. B. Magath. In each case the host was Amiatus calvus. 

Pearse (1924) records A. acuminata from the ‘‘wall-eyed pike” in Lake 
Pepin, Wisconsin, but gives no further data. 


AZYGIA LONGA (LEIDY 1851) 
[Figs. 19, 20 and 30] 


Synonyms: Dist omum longum Leidy 1851 
Dist omum tereticolle of Leidy 1851 
Megadistomum longum (Leidy) Stafford 1904 
Azygia tereticolle of Stafford 1904 
zygia sebago Ward 1910 
Azygia bulbosa Goldberger 1911 
Hassallius hassalli Goldberger 1911 
Azygia lucii of Cooper 1915 

Authentic material of all these forms (with the exception of Stafford’s) 
was obtained. A careful comparative study of this material has led to the 
acceptance of the above list of synonyms. The occurrence of intermediate 
conditions between somewhat extreme types, and the high degree of 
variability of some factors, necessitates the extension of the limits of the 
species as will be shown. In view of the high degree of contractility and 
marked growth changes of trematodes in this group, all comparisons were 
made relative to body length and on the basis of body proportions. Even 
on this basis consideration must be given to relative changes in proportions 
with growth. 

Azygia sebago Ward (1910) from the Sebago salmon is the best described 
of American species. Leidy’s Dist. longum reported in 1851 and the various 
other species recorded from America since 1910 have appeared to differ 
more or less markedly from A. sebago. These differences will now be 
critically examined. 

In separating A. sebago from the European species, A. lucii (=A. tereti- 
colle) Ward emphasized the posterior extent of the vitellaria. Although 
Odhner (1911b) is partially justified in discounting dependence upon 
vitellaria in this genus, the distinction seems to be a valid one. Not only 
in A. sebago, but in all American forms of Azygia examined, the vitellaria 
always extend appreciably beyond the hind testis, usually at least half way 
from this point to the posterior end, and may even reach to the extreme 
posterior tip as was observed in one case. According to descriptions and 
figures of A. Jucii, the vitellaria end in the region of the hind testis and 


64 ILLINOIS BIOLOGICAL MONOGRAPHS [190 


rarely extend appreciably posterior to it, although van Beneden (1858) 
says the vitellaria reach ‘‘depuis la ventouse posterior jusqu’en dessous du 
second testicule.” His figures show the vitellaria extending beyond the 
hind testis to a point about 1/4 the distance between that organ and the 
posterior end. Looss (1894:16) describes their extent for the European 
species as follows: “‘Die Dotterstécke erstrecken sich in den Seitentheilen 
des Leibes ausserhalb der Darmschenkel nach vorn hin nicht bis an den 
Bauchsaugnapfi—sie endigen ungefiihr die Linge seines Durchmessers 
vorher-, nach hinten zu kaum jemals bis iiber hintere Grenze des zweiten 
Hodens hinaus.” 

Further distinction between American species and A. lucii can probably 
be found in pharynx shape, a point upon which Odhner separates a new 
species, A. robusta. The pharynx of American species is more globose than 
the elongate pharynx of A. lucii. This point will be considered in more 
detail under A. robusta. 

A. sebago averages about 6 to 8 mm. in length. Specimens were found 
as small as 1 mm. and no ova were present in forms 2.85 mm. long. In 
regard to sucker proportions: ‘“The ventral sucker or acetabulum is usually 
distinctly smaller than the oral. In the extreme case it appears about equal 
in size or, on the other hand, only about half as large’ (Ward, 1910:1177). 
The questions of body size, size at sexual maturity, egg size, and sucker 
proportion are important points of comparison in American Azygia species. 

Of the other Azygia species, A. bulbosa Goldberger is most evidently 
identical with A. sebago. The descriptions of the two forms show no 
important differences. Type material of both species was studied. Refer- 
ence to comparative tables (Tables 15 to 18) shows almost identical body 
size and proportions, as well as similar position and arrangement of organs. 
Goldberger gives the egg size of A. bulbosa as 56 by 25u. Although the 
eggs may reach a length of 57y, the average of my 110 measurements gave 
the egg size as 48.3 by 28.7yu. Ward gives the egg size of A. sebago as 48 
by 27x. 

The original type material of Hassallius hassalli Goldberger was also 
examined for comparison. That all of this material was strongly contracted 
was made very evident by the ring-like foldings of the cuticula and the 
excessive foldings of the intestine. Goldberger himself explained the 
“numerous transverse sulci’ of the cuticula as “apparently due to con- 
traction of the worm.” The high degree of body contraction is also evi- 
denced by the longitudinal compression of the organs, especially the uterus, 
gonads, and vitellaria. The pharynx is brought down closer to the ventral 
sucker than is normal. Yet, in spite of the evident body contraction, 
Goldberger separates his genus from Azygia on a thicker, shorter body 
form, and a lateral position of the ovary in relation to the anterior testis, 
both of which characters would be caused by body contraction. The only 


191] SOME NORTH AMERICAN FISH TREMATODES—MANTER 65 


comparison Goldberger makes between the two genera is in these words: 
“This new genus, aside from its external characters, differs from Azygia 
in the position of the ovary, which here is by the side of, that is in the same 
transverse plane as the cephalic testis, instead of cephalad of the latter as 
in Azygia.” The shorter and thicker body shape is directly due to con- 
traction. In regard to the position of the ovary, reference need only be 
made to Goldberger’s figure of Azygia acuminata (his Fig. 8) and to the 
following sentence from his description of this Azygia species: ‘‘In one of 
four press preparations, the ovary bears exactly the same relation to the 
testes as that in Hassallius hassalli; that is, it is within the zone of the 
cephalic testis.” In Azygia species as in Otodistomum (see Figs. 13-18), 
the ovary may be located slightly to the right or to the left of the anterior 
testis, and is consequently forced into the “‘zone’’of this testis when the 
body is contracted. Until the ovary can be shown to be lateral to the testis 
in uncontracted specimens, this character cannot be given even specific 
significance. 

In fact, after allowance is made for body contraction, this form cannot 
be distinguished from the other common American forms as represented 
by A. sebago and A. bulbosa. Goldberger’s own description and figures 
show the terminal genital apparatus in his A. bulbosa and Hassallius 
hassalli to be exactly similar. Study of his publication and original material 
reveals not a single point of difference between the two forms, except 
differences that might be due directly to body contraction. Comparison 
of sagittal sections of this species with sagittal sections of A. sebago and the 
A. lucii of Cooper shows no differences that can in any sense be considered 
specific. Goldberger gives an egg size of 48 by 26u measured from sections. 
My measurements of eggs from toto mount gave about 49 by 24y, but the 
larger eggs measured from sections were from 54 to 57y in length by about 
24u in width, or practically exactly the measurements for A. bulbosa. The 
internal parenchyma muscles in Hassallius hassalli are prominent and are 
exactly as in A. sebago and the A. lucii of Cooper. 

Leidy in 1851 described Distomum longum from the mouth of Esox 
estor (=E. lucius). Stafford (1904) designates as ‘‘Megadistomum longum 
Leidy” forms which he collected from the mouth, esophagus, and stomach 
of Esox masquinongy. These trematodes are very long, Leidy’s speci- 
mens being up to 76. mm. (3 inches) in length, while Stafford reports living 
worms as extending to 127. mm. (Sinches), a truly prodigious length. 
Stafford gives a normal length of 75 mm. Both Leidy and Stafford give 
the oral sucker as slightly larger than the acetabulum. Odhner (1911b) 
expresses the view that this trematode should be considered as a large 
Azygia species. Cooper (1915) collecting material from L. masquinongy 
considers his form the same as that reported by Stafford and identifies it 
as Azygia lucit. 


66 ILLINOIS BIOLOGICAL MONOGRAPHS [192 


Study of Leidy’s original Distomum longum and Cooper’s material 
clearly shows that they represent members of the genus Azygia. Their 
large size is certainly not sufficient basis to warrant Stafford in forming 
a genus, Megadistomum. Leidy’s Dist. tereticolle (from Esox reticulatus) 
also was compared with them, and in the single specimen available in the 
Leidy collection, the oral sucker, contrary to Leidy’s description, was 
found to be slightly larger than the acetabulum. In Dist. longum, Leidy 
describes the genital opening as “‘just anterior to the middle of the neck, 
or nearer the oral acetabulum.”’ Such was not the condition in the two 
specimens of this form available. In each case the genital aperture was 
close in front of the ventral sucker, as is, indeed, characteristic of the genus 
Azygia. In the most elongate specimen the esophagus was unusually 
extended longitudinally and at its base a swollen region showed a marked 
resemblance to the cirrus sac. It is possible that Leidy mistook this appear- 
ance for the end-apparatus of the genital system. The true position of the 
terminal genital-apparatus in Dist. longum is seen in Figure 30. 

Cooper also collected Azygia species from the pike (L. luctus). These 
latter trematodes were much smaller in size, and apparently a different 
species, but Cooper, after a careful comparison of his smallest examples 
from the maskinonge with those from the pike, concludes that they repre- 
sent a single species. He also points out the highly variable size at which 
egg production begins. A 14. mm. trematode showed less mature eggs than 
one 6. mm. long from the same host. ‘On the other hand,” Cooper adds, 
“examples of intervening lengths may have their uteri distended with ripe 
eggs!’ (Cooper 1915:192). Forms from the trout were all immature 
although they reached a length of 11 mm. 

This variable size at which eggs are first produced in Azygia species is 
in contrast with the fairly constant size at sexual maturity in Otodistomum 
species. The large number of different hosts in which Azygia species occur 
may be associated with this variability. Another possible factor is the 
season of the year, but the influence of this factor would be difficult to 
determine. Eleven different fish hosts have been reported for the present 
Azygia species. Ward collected his material in July and August and found 
that those forms from the smelt although attaining a length up to 11 mm., 
were always immature. Cooper does not indicate the season of his collection 
but found all forms from the trout and from the small-mouthed black bass 
immature. Stafford examined his fresh water fish in the spring and fall. 
One specimen of his ““Megadistomum longum”’ measured 18. mm. long but 
contained no eggs; and the largest individuals of his ‘‘A. tereticolle’’ were 
smaller than immature individuals of Megadistomum. He found that most 
of his “Mimodistomum angusticaudum” were immature, but “towards the 
end of October” found a few sexually mature. 


193] SOME NORTH AMERICAN FISH TREMATODES—MANTER 67 


Whatever effect the season of collection may have, it is certain that 
what is evidently the same Azygia species does not attain sexual maturity 
at the same time in the different hosts in which it occurs. Thus, while 
average sized forms are producing eggs in such hosts as pike, pickerel, and 
salmon, specimens fully as large are still immature in such hosts as smelt, 
trout, small-mouthed black bass, and perch. 

That.variation in body size at sexual maturity may occur within a single 
host is shown by Cooper’s report of a 14 mm. trematode with less mature 
eggs than were commonly found in specimens 6 to 14 mm. in length. 
Further data is needed, however, to show the extent of this variation. It 
has not been noted by other workers, and certainly is not so conspicuous 
as the marked differences found in specimens from different hosts. 

The maximum body size which the trematode attains also seems 
associated with the host. In those cases wherein the greatest size is reached 
(as in the maskinonge and pike) there also seems to be considerable growth 
before sexual maturity (e.g. Stafford’s immature 18 mm. specimen), and 
it is very possible that the ultimate size which the trematode may reach 
is associated with the amount of growth before eggs are produced, and this 
latter condition may, in turn, depend upon the fish host. 

The following tables (Tables 10-13) show absolute measurements on 
these different forms. The 66 mm. specimen of Dist. longum was very 
highly extended and had apparently been stretched in killing. Moreover, 
the body was not equally extended but was more elongate in the uterus 
region just posterior to the acetabulum. The 37 mm. specimen therefore 
probably furnishes the more normal proportions. 


TABLE 10. Azygia sebago 


Measurements in millimeters 


2 8 8 35.34 
g a) Plo r) cs 2 oa 8 % 3 
3 o of o ov 39 “| Be au = has 
Boies eee loo eles lg] eat} ee | 8s 
S |B \68| 2 |eee 28s 883) 28 | 22 | 22 
5.9 0.9 0.65 | 0.59 2 1.4 0.31 2.12 0.72 0.72 
5.9 0.9 0.65 | 0.59 23 1.4 0.31 212 0.72 0.72 
10. 0.93 | 0.65 | 0.58 4.37 1.9 0.65 2215 Ze 2: 
6.7 1.06 | 0.65 | 0.56 2525 1:5 0.41 2.18 1.31 1.18 
11.5 0.75 | 0.67 | 0.56 4.06 2 0.5 3.75 2.3 2.4 
13%, 0.5 0.74 | 0.56 5.3 2.5 0.9 3.25 1.9 1.9 
9. 1.5 0.68 | 0.62 259. 1.8 0.4 2.8 1.12 0.55 
12. nie | 0.8 0.5 4.8 3. 23412 3.43 1.9 1.9 
10. 0.81 | 0.71 | 0.52 4.18 2.56 1.3 3.18 1.93 2.28 
10.5 0.81 | 0.65 | 0.56 3.6 2.4 1.06 3.37 212; 1.87 


68 ILLINOIS BIOLOGICAL MONOGRAPHS [194 


TABLE 11. Azygia bulbosa 


Measurements in millimeters 


g z| 2.3 | 23 
; a |, 2/22 38.ea $3 | 22) 23 
2 = | se [oe el Se ee sal) ee eae eee 
a SZ |SS] BS |Bss/ Bs gasses] ee] ss] 2S 
4 Fe 168| « ISS Bla “ISSAs AS | FB | Fs 
5,68 | 1. 0.81 | 0.62 2.43 1.68 0.65 1.49 0.75 0.75 
6.3 1.37 | 0.87 | 0.62 Qed, 1.8 0.65 1.5 0.75 0.75 
6.2 1.25 | 0.81 | 0.68 2.4 2.1 0.58 1.6 0.7 0.7 
8.4 2.9 | 1.25.1 1: 2.6 2:5 0.84 2.5 1732, 125 
3.9 0.9 | 0.66 | 0.54 1525 125 0.37 0.78 0.28 0.28 
5.6 0.9 | 0.69 | 0.54 2: 1.6 0.58 1.6 0.73 0.92 
7.1 1.1 | 0.87 | 0.63 2. 2.5 0.69 2.1 ake 1.2 
5.1 1. 0.75 | 0.56 1.68 1.62 0.9 1.3 0.74 0.74 
4.18 | 0.9 | 0.56 | 0.35 1.3 1.49 0.5 1512 0.55 0.55 
6.9 1.1 | 0.81 | 0.62 1.9 2: 0.8 2.3 1.43 1.43 
5.9 1.1. | 0.75 | 0,63 1.9 1.8 1.56 1.6 0.85 0.85 
TABLE 12. Cooper’s Azygia lucii from L. masquinongy 
Measurements in millimeters 
» n n 
25) .8|e2/| 33 
2 8, 818,~(g22| $2 | 22) 22 
S | Sel es (ee ore ae eee le eee ae 
FI ZS (BS) B [Bss[essless| BS] e258] 2B 
4 Se |/Oa] < |@eki[Raesi(aaes| GS | FB | FB 
29. 2.06 | 1.06 | 1.06 15.3 4. 4.8 6.87 S21 4.07 
29. 2a 1d 1.1 12.3 4.4 decd: 9.6 4. 6.1 
39. 2.18 | 1.25 | 1.25 17. 4.3 8.2 9. 5.6 4.4 
31 1.8 | 1. 1 14. 3.68 5.3 9.1 5.23 323. 
2.3 1.25. ||, 1:37 5.12 9.7 
1.87 8.4 6.22 529 
1.68 9.6 A) 6.8 
1.18 | 1.18 
0.87 | 0. 
3.4 0.5 | 0.48] 0.5 * 


The large size of Dist. longum and the form from the maskinonge seems 
at first to separate them from most of the other forms. Leidy’s Disé. 
terelicolle, however, somewhat bridges the gap. 

The equal size of the suckers in the form from the maskinonge is distinct 
in these tables, but Cooper himself reports the oral sucker as larger than 
the acetabulum. In Dist. longum which this form most closely resembles, 
the oral sucker is larger. Moreover, Ward reports occasional equality of 
sucker-size in A. sebago. In view of these facts, the apparently constant 
equality of the size of the suckers in the above form is probably a coin- 
cidence, and at any rate could not alone justify a new species. 


195] SOME NORTH AMERICAN FISH TREMATODES—MANTER 69 


TABLE 13. Cooper’s Azygia lucii from the pike 


Measurements in millimeters 


ww un wn 
Oe no] os r=] = 
2 8,218, ~/$22| 82 | 22] 22 
g 3 ~| 8 oS S/SSs/oSs} of gy gy 
a) oO eens . 4 fe Nae 3 2 ° 
q Ss |8a Br) apmdiasgeslags!] as Ssuiss 3 < 
4 Se |oa| « jagsdlass(as8| o8 | FB | FB 
142 1.6 | 0.93 | 0.75 4.18 Zed 0.25 5. 2.8 2.5 
14. 1.12 | 0.78 | 0.56 6.3 2.9 0.89 5: 251 2.3 
8. 1 0.5 | 0.43 3.75 1.8 0.48 1.75 0.75 0.68 
11. 0.75 | 0.68 | 0.56 4.75 2.5 15 2.68 1.18 1.37 
7.5 0.87 | 0.67 | 0.52 2.9 1.6 0.28 2% 0.9 0.87 
8.5 0.68 0:5 3.4 1.8 0.43 1.4 0.8 0.8 
12. 0.93 | 0.75 | 0.62 5.5 3.9 0.9 2.18 1:5 fy, 
Leidy’s Distomum tereticolle 
20.3 | 0.97 | Ors 0.71 «| 9:3. | 23.9 2.5 | 732 1 36 3.6 


Distomum longum 


1.3 38. | 6.8 18.7 | 12.1 | el RA 
1.131917 5.68 9. 4, 4. 


66. ea 1.42 
37. 12565 J 037 

The egg size is larger in the larger forms, but intermediate sizes were 
found in some of the material from the pike as shown by the following 


measurements. 


TABLE 14 
Average egg sizes in American forms of Azygia 
ASV E10 SCDEZO S oisssieicccs ave ciadtececnneecss 48 by 27 
Asy eta bulbosa: coe s <vu es aiewies diseuersie ses 48 “ 28 
Leidy’s Distomum tereticolle. .........00ceeee 45 “ 28 
Distomum longutt.ocaccsscccvccecsaccevcvece 62 “ 34 
Cooper’s Azygia lucti from maskinonge........ 63 * 33 
Cooper’s Azygia lucii from pike.............. 51 “ 28 
Cooper’s Azygia lucii from pike.............. 56 “ 28 


Two measurements are given in the last case as one trematode from this 


collection showed larger eggs. 

The following tables (Tables 15-18) show the ratios of body length to: 
(1) width, (2) ‘‘neck” region, (3) uterus region, and (4) distance between 
ventral sucker and most anterior vitellaria. 


70 


ILLINOIS BIOLOGICAL MONOGRAPHS 


TABLE 15 


PROPORTION OF Bopy LENGTH TO WipTH IN AzyYGIA SPECIES 
Bopy LENGTH IN MILLIMETERS IS GIVEN IN PARENTHESES 


A. sebago 
6.5 (5.9) 
11.7 (10.5) 
6.2 ( 6.7) 
11.8 (10. ) 
15.3 (11.5) 
26. (13. ) 
6. (959 
10.9 (12. ) 
12.3 (10. ) 


Cooper’s A. lucit 


from pike 
8.7 (14. ) 
12. (14. ) 
14.6 (11. ) 
8.6 (18) 
12.9 (125) 
8. (8. ) 


A, bulbosa A.a 
5.68 ( 5.68) Tish 
4.6 ( 6.3) 7.9 
a ( 6.2) 

3. ( 8.4) 
4.3 ( 3.9) 
6.2 ( 5.6) 
6.5 CA) 
5.1 
4.6 ( 4.1) 
Ayes! ( 6.9) 
4.4 ( 5.9) 
Cooper’s A. lucii 
from maskinonge 


ngusticauda 
( 5.25) 
( 4.9) 


Dist. longum 


14.5 (29. ) 42.2 (66. ) 


14.5 (29. ) 23.5 


17.8 (39. ) 
6.8 ( 3.4) 
TABLE 16 


G7.) 


[196 


A. acuminata 


3. 
3. 
4. 
3. 
4. 
4. 
4. 
the 
3. 
6. 
7. 


wROwWwWOMNWwWUaNININ DA OC 


arey 


( 9.37) 


Leidy’s Dist. tereticolle 


20.8 


(20.3) 


PROPORTION OF THE ToTAL Bopy LENGTH TO THE DISTANCE FROM VENTRAL 


A. sebago 
4.2 (5:29) 
5.2 (10. ) 
4.4 ( 6.7) 
5.7 (11.5) 
52 (13. ) 
5 (3) 
4, (12. ) 
3.9 (10. ) 
4 (10.5) 


Cooper’s A. lucii 
from pike 
2 (14. ) 
8 (14. ) 
4 C8i) 
7 G5) 
4 (11. ) 
7 ( 8.5) 
(12. ) 


SucKER TO ANTERIOR END IN AzyYGIA SPECIES 


A. bulbosa A, angusticauda 
3.3 ( 5.6) Qe ( 5.25) 
3.5 ( 6.3) 25 ( 4.9) 
3. ( 6.2) 

3.3 ( 8.4) 

2.6 ( 3.9) 

3.5 ( 5.6) 

3s Fst) 

2.7 ( 4.1) 

3.4 ( 6.9) 

3.3 ( 5.9) 

Cooper’s A. lucii Dist. longum 
from maskinonge 

pe? (29. ) 9.7 (66. ) 

6.6 (29. ) 6.7 (Giz) 

o (39. ) 

8.3 (31. ) 


Body length in millimeters is given in parentheses 


NNWNNNWNNN » 
NOWWNHHOOR 


. acuminata 


(8. ) 
(11.3 ) 
(10.9 ) 
( 9.75) 
( 9.68) 
( 9.87) 
( 6.87) 
( 6.56) 
( 6.3) 
(7:5) 


Leidy’s Dist. tereticolle 


Died 


(20.3 ) 


197] SOME NORTH AMERICAN FISH TREMATODES—MANTER 71 


TABLE 17 


PROPORTION OF ToTAL Bopy LenctH To LENGTH OF UTERUS REGION 
IN AZyGIA SPECIES 


Body length in millimeters is given in parentheses 


A. sebago A, bulbosa A. angusticauda A, acuminata 
2.9 ( 5.9) 1.9 ( 5.68) 2.8 ( 5.25) 3.6 ( 6.87) 
2:2 (10. ) 2.8 (623: 2.9 (4.9 ) 2.8 ( 6.56) 
239) (Cons) 225 (6:2.) 3.1 (6.3 ) 
2.9 (11.5) D5 ( 8.4 ) 2.8 (Gee) 
2.4 (13. ) 2.3 (3.9 ) 3. G8. .) 
oe (16. ) 2.8 (S26:) 352 (10.9 ) 
2.5 @25) 3.5 Cit) 2.95 ( 9.75) 
2.3 (10. ) 3: CSL) 3.2 ( 9.68) 
2.6 (10.5) 3.2 ( 4.18) 200 ( 9.87) 

3.6 ( 6.9 ) 

Sic (5.9 ) 
Cooper’s A. lucii Cooper’s A. lucii Dist. longum Leidy’s Dist. tereticolle 

from pike from maskinonge 
3.3 (14. ) 1.9 29.) 1.7 (66. ) 2.2 (20.3 ) 
2.2 (14. ) 2:3 (29. ) 1.8 (37. ) 
21 (8...) 2.3 (39. ) 
23 (is) Zs2 (GLa) 
2.6 (7.5) 
QE ( 8.5) 
22 (12. ) 
TABLE 18 


PROPORTIONS OF THE Bopy LENGTH TO THE DISTANCE FROM VENTRAL SUCKER 
To THE Most ANTERIOR VITELLARIA IN AZYGIA SPECIES 
Body length in millimeters is given in parentheses 


A. sebago A, bulbosa A, angusticauda A. acuminata 
19. ( 5.9) 8.7 ( 5.68) 26.2 ( 5.25) 20. (8: ) 
14.4 (13. ) 9.7 (6:35) 2152 ( 4.9 ) 17.3 (11.3 ) 
16.7 ( 6.7) 10.6 ( 6.2 ) 29.4 (10.9 ) 
2235 (9.1) 10. ( 8.4 ) 19.5 (9.7 ) 
15.5 (12. ) 9.6 (3.6) 28.2 (9.8 ) 
520 (19. ) 10.5 (3.9) 322 ( 9.68) 
23. (11.5) 10.2 (wet) complete (6.8 ) 
135 (10. ) Sak CS:1°) 13.1 ( 6.56) 
9.9 (10.5) 8.3 ( 4.18) 28.6 ( 8.87) 
8.6 ( 6.9 ) 12.5 ( 9.37) 
10.5 (5.9°) 22: (t..°) 
complete (6.3 ) 
complete (7.5 ) 
Cooper’s A. lucii Cooper’s A. lucit Dist. longum Leidy’s Dist. tereticolle 
from pike from maskinonge 
45. (14. ) 6. (29. ) 3.5 (66. ) 8.1 (20.3 ) 
15.7 (14. ) 3.8 (29. ) 
16.6 C8e) 4.7 (39. ) 
03 (11. ) 5.8 (31.2) 
26.7 ( 7.5) 
19.7 ( 8.5) 


137. (12. ) 


72 ILLINOIS BIOLOGICAL MONOGRAPHS [198 


The relative width of the body is seen to be quite variable. Differences 
can be explained by different degrees of contraction, and by growth 
changes. The closely related genus, Otodistomum, has been shown to 
increase greatly in length but very little in width with growth. This 
condition is well shown by reference to the 39 mm.-and the 3,4 mm. 
specimens (Table 12) from the maskinonge. In the former case the length 
is 17.8 times the width while in the latter the length is only 6.8 times the 
width. 

Dist. longum and the form from the maskinonge have body lengths 
7 to 9 times the neck regions, while in the other forms this ratio varies 
from about 3 to 5. But this difference is of no specific significance, being 
clearly due to the larger size of the former trematodes and representing 
a change in ratio which has been shown to occur with growth in similar 
forms. That is, the proportions shown in the table are what would be 
expected if all the forms represented different stages of growth of the same 
species. In the 66 mm. specimen of Dist. longum some allowance should 
perhaps be made for artificial extension which the other specimens did not 
receive. 

The tables dealing with the uterus length and with the anterior extent 
of the vitellaria both indicate a slight tendency in Dist. longum to differ 
from the other species. In regard to uterus length, however, the smallest 
ratio (1.7) or longest uterus is in the specimen already described as showing 
a localized extension in that region. Furthermore, a tendency for this 
region normally to increase slightly its proportion to the remainder of the 
body was shown to be true in Otodistomum. 

The anterior extent of the vitellaria is highly variable, as the body may 
be from 3.5 to 45 times the length of the distance between vitellaria and 
the acetabulum. Because of this high variation and because there is no 
consistency in any single group outside of A. acuminata, this point cannot 
be urged in separating species. 

Thus, in spite of the great difference in size, a consideration of the 
possible features which might separate these species shows that there has 
been found no valid basis for distinction between them. It is especially 
significant that, except for characters which vary and overlap in the 
different forms, all the differences are in the direction taken by normal 
growth changes, and are moreover commensurable with such changes. 
Therefore, one feels justified in concluding that so far as can be determined 
morphologically, all these forms are representatives of the single species, 
Azygia longa (Leidy), and that this species manifests a variety of states, 
the extremes of which differ widely, but all of which are in accordance with 
growth changes and capacities known in related trematodes. The following 
fish are known hosts: Salmo sebago, Osmerus mordax, Esox reticulatus, 
Anguilla chryspa, Perca flavescens, Esox lucius, Amiatus calvus, Esox 
masquinongy, Salvelinus namaycush, Lucioperca sp., Micropterus dolomieu. 


199} SOME NORTH AMERICAN FISH TREMATODES—MANTER 73 


AZYGIA ROBUSTA ODHNER 1911 


Odhner (1911b) established the species, A. robusta, ‘‘mit einer gewissen 
Reserve.”” This form (from the salmon) differs from A. lucii apparently 
in attaining a somewhat greater length (to 47 mm.) and in possessing a 
spherical although ‘‘mitunter etwas langer als breit’’? pharynx. The latter 
feature is the chief one upon which the species is founded. Odhner in his 
“‘ziemlich reichlichen Material’ never finds the pharynx twice as long as 
wide, while in the material (A. Jucii) from the pike, the pharynx is never 
spherical but always elongate. In a postscript, Odhner claims a substantia- 
tion of this new species on the character of the pharynx. As he gives no 
further specific differences between the new species and A. /ucii it is to be 
inferred that the two are similar in other respects. 

This distinction on pharynx shape introduces a new possible taxonomic 
factor for the group. The following measurements from favorable total 
mounts and cleared specimens might help in estimating the value of this 
character. The longitudinal axis of the pharynx is the first measurement 
given in each case. All measurements are in millimeters. 


Otodistomum cestoides 


0.54. 0.39 0.48 X 0.39 0.37 X0.24 
0.56 X 0.37 0.71 X 0.56 0.35 X 0.26 
0.46 X0.41 0.54 0.50 0.43 X 0.37 
0.18 X0.18* 0.50X 0.29 0.37 X0.37* 
0.24 X 0.16 0.18 0.15 0.35 X 0.28 
0.20X0.18F 0.56 X 0.39 0.56 X 0.46 
0.18 X 0.167 0.24 0.18 0.74 0.56 
0.22 X 0.16 0.52 0.43 0.74.X0.74* 
0.18 0.15 0.46 X 0.35 0.44X0.31 
0.46 X 0.37 0.37 0.29 

A. sebago A. bulbosa A, acuminata 
0.35 X 0.20 0.31X0.31* 0.41 X 0.26 
0.28X0.37* 0.20 0.22* 0.37 X 0.35 F 
0.18X0.11 0.37 X0.41* 0.37 X0.31 
0.37 X 0.20 0.29X 0.22 0.18 X0.18* 
0.46 X 0.28 0.29 X 0.28 0.27 X0.27* 
0.28 X0.18 0.41 0.41* 0.31 0.24 
0.37 X0.28 0.46 X 0.45 T 
0.28 X0.22 
0.28 X 0.20 


0.20 0.14 


74 ILLINOIS BIOLOGICAL MONOGRAPHS [200 


A. loossii Cooper’s A. lucii Dist. longum Leidy 
0.18 0.14 0.62 X 0.37 0.65 X 0.50 
0.18 X0.14 0.65 X 0.43 0.65 X 0.46 
0.18 X0.13 0.48 X 0.29 

0.37 X0.27 
0.40X0.31 
0.37X 0.344 
0.32 X0.27 


* indicates that the pharynx is at least as wide as long. 
{ indicates that the pharynx is practically as wide as long. 


A study of these figures shows that in no American species does the 
pharynx measure twice as long as wide; that it is ovoid rather than cylindri- 
cal; and that in all cases it may assume an almost spherical shape. For the 
European species, A. /ucii, Looss (1894) describes the pharynx as cylindrical 
and his figure shows its length to be twice its width. Of this species Odhner 
(1911b:520) says: ‘‘Pharynx immer langgestreckt, etwa doppelt so lang 
wie breit, bei 18-22 mm. langen Exemplaren 0.6-0.8 mm. lang und 0.35- 
0.45 mm. breit.’’ Accepting these records, there appears to be rather definite 
difference between A. /ucii and all American species in the shape of the 
pharynx. Odhner’s A. robusta resembles the American species in this 
respect. In view of the range of variability shown by the above measure- 
ments, this feature becomes of questionable specific value, particularly 
when considered alone. But until further comparisons with numerous 
specimens of European forms are made, the conclusions of Odhner will be 
accepted. 


AZYGIA PERRYIT FUJITA 1918 


Fujita (1918) described this species from a fresh-water fish, Hucho 
perryi Breevoort, sent him by a friend. Fujita found the trematode 
attached to the external surface of the fish especially to the pectoral fin, 
oral cavity, buccal cavity, and outer and inner surfaces of the operculum 
and gills. This location of the parasite, although emphasized by Fujita, 
is, of course, of no significance since Azygia species normally inhabiting the 
anterior regions of the digestive system often migrate forward into the oral 
cavity and hence to the exterior. Such migration was noted as conspicuous 
in A. sebago by Ward (1910). 

Fujita compares a few relative measurements of his form with A. lucii 
and A. sebago. His table of comparison follows. The figures are in per- 
centages presumably based upon body length. 


201] SOME NORTH AMERICAN FISH TREMATODES—MANTER 75 


A. perryii Average A, sebago Average | A. lucii 

Distance between 

oral and ventral} 18 19 17 18 18 18% 16 22 24 11 19 18% 24 
suckers 

Distance from an- 

terior tip to center 

of ovary 54 53 47 50 49 51%* | 54 56 54 63 66 59% 63 
Center of ovary to 

center of post. tes- 

tis 62 59 59 57 58 59%* | 65 65 66 77 74 69% 74 
Breadth behind 


ventral sucker 14 14 14 12 15 14% 16 21 17 6 19 16% 8 


* These two numbers are interchanged in the original table, but it is obvious that this 
is due to misprinting. 

Fujita concludes from these figures that his species “‘has a resemblance 
to the American species in the distance between suckers and breadth of 
body, but in the location of the reproductive organs, which is very im- 
portant, it is entirely different from the American species. On the other 
hand, the European species resembles closely the American species in 
positon of reproductive organs, and on other points it differs from both 
American and Japanese forms.’ He does point out that these percentages 
are of comparative value only, since they will vary according to the 
methods used in preserving the specimens. 

But Fujita’s conclusions from his table are open to still more serious 
objections. The number of specimens compared is small as measurements 
of the single case of A. /ucii were calculated from the figure by Looss (1894). 
Furthermore, all of the characters considered are influenced by different 
degrees of contraction and a contraction of any particular region of the 
body would alter such percentages. This fact might account for the high 
variation in the figures for A. sebago. But still more important, an analysis 
of the figures as they stand shows no valid differences between the three 
forms. The figures for A. sebago cover a range which includes figures for 
both the other forms in every character considered except “‘center of ovary 
to center of posterior testis’’ where 62% in A. perryii is the nearest approach 
to 65% in A. sebago. It is quite unexplained how ‘‘the position of the re- 
productive organs” in A. perryii is “entirely different” from the other two 
species. The derivation of the percentages in the character dealing with 
this distance from the ovary to the posterior testis is also not clear. The 
percentages (62% to 74%) certainly cannot be in relation to body length 
as the other figures appear to be, and 6.2% to 7.4% likewise are inappro- 
priate for such ratio. 


76 ILLINOIS BIOLOGICAL MONOGRAPHS [202 


Two type specimens of A. perryii in the Ward Collection* were available 
for study. Measurements of these specimens are as follows: 


Length 8.6 mm. 5.6 mm. 
Width 1.3 0.8 
Oral sucker 0.78 0.58 
Acetabulum 0.6 0.48 
Post. edge acetab. to mid. ovary 2. 1.06 
Post. edge acetab. to anterior end 2.18 1.8 
Post. edge acetab. to most ant. | right: 0.18 0.09 
vitellaria left: 0.56 
Post. edge testis to post. end 3.1 1.9 
Vit. on left beyond testis 0.74 0.84 
Vit. on right beyond testis 0.2 *1.3 
Pharynx 0.317 0.24 
x x 
0.28 0.11 


Fujita figures the vitellaria as terminating posteriorly in the immediate 
neighborhood of the posterior testis. I found that the posterior extent of 
the vitellaria was only slightly beyond the testis in the 8.6 mm. specimen, 
although they extended slightly over 1/2 the distance between this point 
and the posterior end on one side only in the 5.6 mm. specimen. In respect 
to this important point, Fujita says: ‘The posterior extent (of the vitel- 
laria) extends somewhat farther down than the posterior testis” and adds 
that the vitellaria “do not extend posteriorly as far as in the American 
form.”’ Since it has been seen that the vitellaria in A. Jucit may extend 
some distance beyond the hind testis, it is apparent that A. perryiz is like 
A. lucii and different from the American species in this respect. 

Concerning the anterior extent of the vitellaria, Fujita says they reach 
“to near the posterior end of the ventral sucker,”’ and concludes that this 
limit is further anterior than is reached by the European species. Looss 
describes them (in A. lucit) as failing to reach the acetabulum by a distance 
about equal to its diameter (his figure shows them ending posterior to such 
a point), and this is about their anterior extent as figured by van Beneden 
(1858). Although in the Japanese material they reach somewhat nearer 


* Collection of Dr. H. B. Ward, vial No. 18.83. 


203] SOME NORTH AMERICAN FISH TREMATODES—MANTER 77 


the acetabulum, the slight difference in this extent could not separate 
Fujita’s form from the European. 

Pharynx measurements of the two specimens in the above table showed 
one elongate pharynx and one ovoid. Fujita gives 0.29 by 0.2 mm. 

Fujita’s egg measurement was 0.058 by 0.033 mm. which is larger than 
the egg size in A. sebago, but about the size attained in the American form 
from the pike. Looss gives 0.045 by 0.023 mm. for A. Jucit. Hence, in egg 
size the Japanese appears to differ from the European form, but that this 
distinction may not be a valid one has been indicated in the preceding 
comparison of American forms. 

Fujita records the presence of the internal longitudinal muscies as 
described by Ward. He noted also that these muscles were located much 
more deeply (i.e., farther from the surface) on the dorsal side than on the 
ventral side. Thus, dorsally the cortical body region measured 0.21 mm., 
while on the ventral side this same region measured only 0.13 mm. in 
thickness. Such a condition was not true in American forms I studied. 
Leuckart’s diagram of a cross-section of A. /ucii is like A. sebago in respect 
to position of these muscles. Some variation in their position is probably 
accidental. 


AZYGIA VOLGENSIS (V. LINSTOW) ODHNER 1911 


Synonyms: Ptychogonimus volgensis v. Linstow 1907 
Distomum volgense (v. Linstow) Liihe 1909 


Odhner states that this species (from Lucioperca sandra) appears to be 
a true form. Apparently only very few specimens are known, v. Linstow 
studying only one. ‘‘Liihe’s (1909) description is based on von Linstow’s. 
Odhner (1911b) does not state the number or source of specimens he 
studied. His description is, however, very brief.’’ It is certainly very close 
to A.lucii and no important distinction can be determined between the two 
from their descriptions. The length of A. volgensis is 5 mm. according to 
Odhner, and 6.2 mm. according to v. Linstow. Odhner contrasts ‘‘Eipro- 
duktion” in A. volgensis at 2 mm. with this condition at 5 to 6 mm. in A. 
lacit, an entirely meaningless feature, in view of the variation the condition 
shows in American forms. These two European species should be further 
studied. On the basis of present evidence A. volgensis must be regarded as a 
doubtful species. 


78 ILLINOIS BIOLOGICAL MONOGRAPHS [204 


SYNOPSIS OF THE GENUS AZYGIA 


A key to the species of Azygia (including the several doubtful European 
species which might represent the single form, A. /ucii) follows: 


Vitellaria not extending appreciably posterior to the hind testis 


Body length about 6 mm.; sexually mature at 2mm.............2 A. volgensis (v. Linst.) 

Body length up to 30 mm. or more 
Pharynx elongate, twice as long as wide; eggs 45 by 23u........2 A, lucit (Muell.) 
Pharynx’ plobose;, CPSP in. cnee swan aeovan «sees «eee es A. robusta Odhner 
BEES: SBE Dy Soe nce ee rete ey eel cere eee eae eee ae A. perryit Fujita 


Vitellaria extending considerably posterior to the hind testis, usually at least half way between 
this point and posterior end of body 

Acetabulum near middle of body; gonads near posterior tip..A. angusticauda (Staff.) 

Acetabulum distinctly nearer the anterior end; gonads anterior from posterior tip by 
about 1/3 ot 1/4 the body length 

Body relatively wide; vitellaria beginning close behind acetabulum; neck usually 

constricted; internal parenchyma muscles weak; eggs about 64 by 33u.... 

ssid eg aveetetaiadeadan gua Neb ei te oes er alior toy eae ny rears en years Mee aleve A. acuminata Goldberger 

Body often extremely elongate; vitellaria usually beginning some distance posterior 

to acetabulum; internal parenchyma muscles strongly developed; eggs variable 

in size (up to 63u in length), usually about 48 to 55u by 28 to 30u........ 

Silas acy ho neas lal SVMS Aaa ee ete ARE EAE coe ore ats ee eee A. longa (Leidy) 


205] SOME NORTH AMERICAN FISH TREMATODES—MANTER 79 


A GENERAL STUDY OF SOME MARINE FISH TREMATODES 


Most of the following trematodes were collected at the Mount Desert 
Island Biological Laboratory during the summer of 1924. A brief account 
of these parasites has already been published (Manter 1925). The following 
descriptions give more complete data on them. A few trematodes from fish 
of the Woods Hole region are also considered. The study of these forms is 
based on specimens from the collection of Dr. Henry B. Ward. Extended 
descriptions are given only to those forms which are new or which have 
been briefly or incompletely described in the literature. Following the 
systematic arrangement adopted by Nicoll (1915) for trematodes of British 
fish, the forms studied would be grouped as follows: 


Order: DIGENEA 
Sub-order: Prostomata 
Super-family: Distomata 
Family: Allocreadiidae 
Sub-family: Allocreadiinae 
Genus: Podocotyle 
1. P.atomon 
2. P.olssoni 
Sub-family: Stephanochasminae 
Genus: Stephanochasmus 
1. S. baccatus 
Sub-family: Lepocreadiinae 
Genus: Lepidapedon 
1. L.rachion 
2. L. elongatum 
Genus: Homalometron 
1. H. pallidum 
Family: Zoogonidae 
Sub-family: Lecithostaphylinae 
Genus: Steganoderma 
1. S. formosum 
Family: Siphoderidae* 
Genus: Siphodera 
1. S. vinaledwardsii 
Family: Azygiidae 
Genus: Otodistomum 
1. O. cestoides 
Family: Hemiuridae 
Sub family: Hemiurinae 
Genus: Hemiurus 
1. H.levinseni 


* Odhner may be correct in not recognizing this family. 


80 ILLINOIS BIOLOGICAL MONOGRAPHS [206 


Sub-family: Sterrhurinae 
Genus: Brachyphallus 
1. B.crenatus 
Sub-family: Lecithasterinae 
Genus: Lecithaster 
1. L. gibbosus 
Genus: Aponurus 
1. A. sphaerolecithus 
Sub-family: Syncoeliinae 
Genus: Derogenes 
1. D.varicus 
Genus: Genolinea 
1. G. laticauda 
Genus: Gonocerca 
1. G. phycidis 
Sub-family: Accacoeliinae 
Genus: Hirudinella 
1. H. fusca 
Unclassified genus: Deropristis 
1. D. inflata 
Order: MONOGENEA 
Family: Tristomidae 
Sub-family: Acanthocotylinae 
Genus: Acanthocotyle 
1. A. verrilli 
Family: Octocotylidae 
Sub-family: Octocotylinae 
Genus: Dactycotyle 
1. D. minor 


THE GENUS PODOCOTYLE 


Stafford (1904) records “‘Sinistroporus simplex Rud.” from seven 
different Canadian marine fish. He comments: “‘.... genital pore to the 
left from the origin of the caeca in all specimens examined,” and on this 
basis seems to found the new genus, Sinistroporus. The species is evidently 
the Dist. simplex Rud. that Linton describes from various fish of the Woods 
Hole region. The sinistral position of the genital pore is not sufficient, 
however, to separate the form from the genus Allocreadium in its older 
sense. Odhner (1905) considers Dist. simplex Rud. as probably synonymous 
with Podocotyle atomon (Rud.) and he also includes Dist. simplex Rud. of 
Levinsen (1881) as a synonym. Odhner redescribes the genus Podocotyle 
with Dist. atomon Rud. as type. 

Podocotyle, originally a sub-genus of Dujardin’s, was listed as a genus 
by Stossich in 1892. Stiles and Hassall (1898) established as type of this 
genus Dist. angulatum Duj. This species is, however, a species inquirenda, 
and Liihe (1900:491) remarks: Das endgiiltige Schichsal der Gattung ist 
demnach abhingig davon, dass diese Spec. inquir. einmal wieder gefunden 


207] SOME NORTH AMERICAN FISH TREMATODES—MANTER 81 


und dann auch wieder erkannt wird.”” According to Odhner (1905:321) this 
type material has been permanently lost, and the species is insufficiently 
described. He therefore assign: Dist. atomon Rud. as type species of 
Podocotyle. At any rate, the forms described as Sinistroporus are without 
doubt members of this genus as separated from Allocreadium. Such a 
synonymy is recognized by Nicoll in 1909 when he lists Sinistroporus 
Staff. as synonymous with Podocotyle (Duj.) Odhner. In an earlier paper 
Odhner (1901) had considered Allocreadium atomon (Rud.) as a highly 
variable species and recognized three varieties. In 1905, he determines 
Podocotyle atomon (Rud.) (=Allocreadium atomon (Rud.) Odhner 1901, 
e.p.) as a fixed species and his earlier varieties he considers as true species. 

The diagnosis of the genus Podocotyle as given by Odhner (1905) is as 
follows: ‘Body elongate, quite evenly wide, sometimes flattened and 
ribbon-like, sometimes cylindrical. Esophagus at most twice as Jong as 
pharynx, forking in front of the ventral sucker. Genital pore to the left, 
lying at the level of the esophagus. Excretory vesicle reaching to the 
ovary. Cirrus-sac elongate, reaching at maximum as far as half way 
between ventral sucker and ovary. Seminal vesicle long, coiled. Pars 
prostatica lacking. Cirrus of marked length, straight. Ovary three-lobed. 
Vitellaria normally not reaching anterior to ventral sucker. Eggs without 
filament. In intestine of marine fish. Type species P. atomon (Rud.) 
Other species, P. reflexa (Crep.), P. olssoni Odhner (= Dist. simplex Olss. 
1868 e.p.).” 

Odhner refers to Linton’s form as either identical with P. olssoni or 
closely related to it. Two species of Podocotyle were found in the present 
collection and these tend to confirm the constancy of the specific nature of 
the characters given by Odhner. In P. atomon the vitellaria are unbroken 
and do not come together between the testes; the testes are relatively 
small, not occupying over one half the cross-section of the body; the 
esophagus is longer than the pharynx; and the cirrus sac over-reaches the 
ventral sucker by a short distance. In both P. reflexa and P. olssoni, the 
vitellaria are broken near each testis and come together between these 
organs; and in both species also the testes are large, occupying a great 
part of the body in cross-section. P. reflexa differs in being cylindrical. It 
also has an esophagus longer than the pharynx. P. olssoni possesses and 
esophagus only as long or even shorter than the pharynx; and has a seminal 
vesicle reaching about half way between ventral sucker and ovary. 


PODOCOTYLE ATOMON (RUDOLPHI 1802) 
[Fig. 49] 
From intestine, Pholis gunnellus (Butterfish) 
From intestine, Anarrhichas lupus (Wolf fish) 
One specimen of this species was taken from each of two butterfish of 
ten examined. These trematodes measured 2.37 mm. and 2 mm. in length. 


82 ILLINOIS BIOLOGICAL MONOGRAPHS [208 


Both of the specimens agreed in detail with Odhner’s description of the 
species, with long esophagus, small testes, and unbroken vitellaria (Fig. 49). 
In one specimen the body was somewhat contracted and in this case the 
esophagus coiled somewhat instead of shortening with contraction, so that 
its length could be easily distinguished as about twice that of the pharynx 
Cooper (1915) reports one young specimen of Sinistroporus simplex from 
the butterfish, but it is very probable that he was dealing with the same 
species now being considered. Both of the present specimens were fully 
mature. 

The single specimen from the wolf-fish measured 3.06 mm. in length 
and 0.57 mm. in width. The esophagus was twice the pharynx length. 
The testes occupied about half the body width and were slightly lobed or 
crenulated as Cooper noted for Sinistroporus simplex. There was a slight 
break in the vitellaria opposite the hind testis, and the follicles approached 
each other between the testes. In these respects, the form showed a 
tendency to assume characters of P. olssoni, although these features are 
more marked in the latter species. In view of this possible variation of the 
vitellaria, the esophagus length seems to be the most useful distinction 
between the species. 


PODOCOTYLE OLSSONI ODHNER 1905 
[Fig. 50] 
From intestine, Urophycis tenuis (Hake) 
- # Myxocephalus groenlandicus (?) (Sculpin) 
¢ & Gadus callarias (Cod) 
¢ be Microgadus tomcod* (Tomcod) Woods Hole 
This trematode is a very common species. Fig. 50 shows the typical 
appearance of the material from the hake. The differences between this 
species and P. atomon have already been pointed out. The specimens from 
the hake show these differences most constantly and clearly. The esophagus 
is short (not longer than the pharynx); the seminal vesicle reaches to a 
point about half way between ventral sucker and ovary; the testes are 
large; and the rows of vitellaria are broken opposite each testis. The size 
was from 2.8 to 4 mm. in length by 0.4 to 0.58 mm. in width. The ventral 
sucker is prominent, usually somewhat protruded, and longer in its cross- 
diameter. It is almost exactly twice the size of the oral sucker. In one 
specimen the body wall about the sucker formed a slightly projecting fold 
around the sucker. 
Material from the cod (which were of small size) agrees with the Woods 
Hole material from the tomcod. These forms show a few slight differences 
from the clear-cut specific characters of the form from the hake. The short 


* Collection of Dr. H. B. Ward, vial No. 13.75. 


209] SOME NORTH AMERICAN FISH TREMATODES—MANTER 83 


esophagus, however, is a constant character in which all agree.The breaks 
in the rows of vitellaria can usually, but not always, be discerned in the 
cod trematodes. The one or two cases wherein the follicles appeared con- 
tinuous were of somewhat contracted specimens. The forms from the cod 
were all small in size. They measured 1.28 to 1.6 mm. by 0.26 to 0.3 mm. 
The seminal vesicle did not quite reach to a point half way between ventral 
sucker and ovary. 

All of these forms also show two regions of slight body contraction, one 
about at the level of the posterior testis, the other usually slightly in front 
of the anterior testis. Figure 50 shows this condition only slightly evident. 
Sometimes it is conspicuous. Odhner does not mention it, nor does Linton, 
although the condition is shown in the figure of his Dist. simplex from the 
tomcod (Linton 1898, pl. 47, fig. 3). From Linton’s description and figures 
there can be no doubt that his Dist. simplex (Linton 1898:525) is the same 
species as the present form from the tomcod. Linton records a length up 
to 2.4 mm., which approaches the size of the material from the hake. The 
egg size in all forms agrees, being 70 to 80 by 37 to 40u. Considering the 
above characteristic features, there can be little doubt that all the forms 
belong to the species, P. olssont. 


STEPHANOCHASMUS BACCATUS NICOLL 1907 
[Figs. 51-52] 
From intestine, Hippoglossus hippoglossus (Halibut) 
Five specimens of this trematode were obtained from the intestine of 
a single halibut. The largest specimen containing about 12 eggs measured 


2.18 mm. in length. The smallest containing one imperfect egg was about 
1.3 mm. in length. Measurements on the large specimen are as follows: 


Weng thier cisraiic amyaukers cine tio toe avs nig ee eee 2.187 mm. 
DW Seta coz cacere sca Aunty srereen ete eres RIM ee FeO 0.467 
Orallisucket Pim aasae waters weete ee a akieaes 4 oe 0.176 
Ventral suckerse. s,s access ate e sit sceucjssscarsluve wie vives 0.256 

ITS PAA LY UK ve yraterevay aves: thecnie dlsniedin as clancis:Scelesoyer coast acon 0.2 

LE TE 0: ae eee eR CRE ERIC Odea Cae care ence mera 0.199 by 0.119 
gS cn nnctaa cose Gaedapecntsseeat aoe e 85 to 91 by 45 to Sip 
Length of spines in posterior row...........0.0cce eee eeee 34 
Length of spines in anterior row..............00.ceeeeeeee 28p 


In two specimens the number of spines in the oral ring was 29, but that 
this number may vary is shown by the fact that only about 25 spines were 
found in a third specimen. Nicoll found from 28 to 30 spines. The ring is 
unbroken, and the spines in the posterior ring are larger than those in the 
anterior ring. 

The characteristic shape of the egg with one pole flattened was noted 
(Fig. 52). This condition at first seemed due to contraction, but Nicoll 


84 ILLINOIS BIOLOGICAL MONOGRAPHS [210 


reports it as specifically characteristic. In cross-section the eggs show a 
peculiar star-shaped outline (Fig. 52), which is evidently characteristic 
for all species in the genus. 


LEPIDAPEDON RACHION (COBBOLD) STAFFORD 1904 
[Figs. 45-46] 


Syn.: Lepodora rachiaea (Cobbold) Odhner 1905 

From intestine, Melanogrammus aeglifinus (Haddock) 

This trematode is fairly common and well known. Nicoll and Lebour 
each report it as common in the haddock of the English coast. Infection, 
however, is always light, usually only from one to three trematodes being 
found in a host. Its presence might accordingly be easily overlooked. In 
the present collection, two specimens were found from one host, and one 
each from two others. It is reported by Stafford (1904) from the same host. 
Stafford gives it the new generic name, Lepidapedon (for the form pre- 
viously known as Dist. rachion Cobbold), but gives no description. Odhner 
(1905) gives a complete and carefully worked out description of the form 
which he named Lepodora rachiaea (Cobbold). In spite of the extent of 
Odhner’s work, Stafford’s name, Lepidapedon, holds priority and has been 
accepted by Nicoll and others. Stafford gives the measurement of 5 by 
1 mm., but my specimens agree more nearly with those of Odhner who 
gives a length of 1.5 to 3.5 mm. with a width varying from 1/5 to 1/4 this 
measurement. The following measurements show general proportions: 


Length ccccicccciciaios sais ce ceaeiee aise ss 2.59 mm. 
Widtheeomaa cee ree eerie ee oniae ee 0.46 
Oralisucker scythe sapoee oe maees 0.24 
Ventralisuckerss srasreieiniessteres srmrcroteyenccnrsin suakete 0.18 
PYe-PHAT YDS secre iiercrsvale clerererereielel orereaishe ies hye 0.285 

PH ary xs 5, eievelsciereseciess cre aiole astvarecccatscaiete 0.19 by 0.17 
XM-diameter, OVATY:. oie ssc is.t oh aes eesecies ee. 0.11 
X-diameter, ant. testis.................0008 0.17 
X-diameter, post. testis...............000-- 0.17 
Length, semi: VeSieccis ceca eacccanee elses 0.285 
GIrrOS'SaCe cn seserss aiaticoe ates see atseinesetvek ee 159 by 114u 
SRS aia) aie ends nsa praessieiacaiere « wbee sin ielasase unites 65 by 34y 


The morphology of the species is well known and the present material 
showed no new features. Most characteristic is the glandular mass of cells 
surrounding the seminal vesicle, and the location of the vitellaria ventral to 
the intestinal ceca. 

Two other species of this genus have been described. Leiper and 
Atkinson (1915) describe a trematode which they name Lepodora garrardi. 
The corrected name would be Lepidapedon garrardi (Leip. and Atkin.). 
The description is not complete in regard to some points and indicates 


211) SOME NORTH AMERICAN FISH TREMATODES—MANTER 85 


(as the figure also shows) that their form approaches the genus Lepo- 
creadium which it resembles in body shape and shortened pre-pharynx. 
No mention is made of any glandular cells surrounding the seminal vesicle. 

Odhner mentions one other species but does not describe it. Miss 
Lebour in 1908 names a species Lepodora elongata (= Lepidapedon elongatum 
(Lebour)), and this species she suggests might be the form mentioned by 
Odhner. It differs from L. rachion by being more elongate in form, possess- 
ing a long esophagus, and with somewhat less extensive vitellaria. Several 
specimens, agreeing in most of these points are found in the present 
collection and were referred to this species. 


LEPIDAPEDON ELONGATUM (LEBOUR 1908) 
[Figs. 47-48] 

Syn.: Lepodora elongata Lebour 1908 

From intestine, Urophycis tenuis (Hake) 

Five specimens were collected from one out of three fish examined. 
The trematode shows close resemblance to L. rachion in general form, 
shape, arrangement of organs, and spiny cuticula, but differs from it in the 
length of the esophagus, extent and position of the vitellaria, and develop- 
ment of the glandular cells about the seminal vesicle. Also, the genital 
pore in this species is closer to the ventral sucker than in L. rachion. These 
same differences separate Miss Lebour’s Lepodora elongata from L. rachion. 
The present form differs only in not being more elongate than L. rachion, 
but this point is one which may be influenced by age of the parasite or by 
body contraction. Typical measurements are as follows: 


Wen pthc cise cic-aatieecsvesere ak 2.4 mm. 
Widths icc celes siecie terciole ot area 0.54 
Orallsuickerz 2.2 bac snsiecs passe Sass 0.119 
Ventral sucker, ...eeicass scons es 0.14 

Pre- pharynx e154 Peciaiack haenisis 0.125 
IPbarynx tegen es eect fucose nies 0.09 
SOpha gus cesiecic a vieve tease era sere Soe 0.091 
X-diameter, ovary.............. 0.29 
X-diameter, ant. testis........... 0.31 
X-diameter, post. testis.......... 0.37 


Miss Lebour does not record the position of the vitellaria in relation 
to the ceca. As has been noted, in L. rachion the vitellaria are ventral to 
the ceca. In the present form, this condition did not hold but the vitellaria 
were found distributed on both sides of the intestine. They extend an- 
teriorly at least to the ventral sucker in L. rachion, but fail to reach the 
level of this sucker in L. elongatum. Another conspicuous difference 
between the two species is found in the character of the glandular mass 
surrounding the seminal vesicle. The cells in this mass are large, globular, 


86 ILLINOIS BIOLOGICAL MONOGRAPHS [212 


and numerous in L. rachion (Fig. 46), but are much reduced in L. elongatum 
where they are very inconspicuous (Fig. 47). In this respect, L. elongatum 
approaches the related genus Lepocreadium. My material also resembles 
Miss Lebour’s and differs from L. rachion in that the testes are separated 
from each other by a distinct space. The pharynx is considerably smaller 
than in L. rachion. 


HOMALOMETRON PALLIDUM STAFFORD 1904 
. [Figs. 54-56] 


From intestine, Fundulus heteroclitus 


This species is the same form referred to by Linton (1901:422, pl. 32, 
Fig. 354) and named Homalometron pallidum by Stafford in 1904. Stafford 
does not describe the genus or species, merely referring to Linton’s paper. 
Linton’s description is as follows: 

“Body very minutely spinose, white translucent; acetabulum and oral 
sucker about the same size; outline of body, long oval; neck short, continu- 
ous with body; greatest breadth in region of testes, near posterior end; 
ecaudate; acetabulum sessile; rami of intestines simple, elongate; esopha- 
gus as long as pharynx; testes two, in median line behind uterus; seminal 
vesicle dorsal to ovary and posterior border of acetabulum; ovary between 
acetabulum and testes, on right side; pharynx sub-globular; genital 
aperture in front of acetabulum, on median line; vitelline glands lying at 
posterior end and along sides of body as far as acetabulum; ova, few, 
relatively large. Dimensions of specimen in formalin, given in millimeters: 
Length 2.72; breadth, anterior 0.43, at acetabulum 0.89; middle 1.07, near 
posterior end 0.36; diameter of oral sucker 0.26; diameter of acetabulum 
0.29; diameter of ovary 0.21; diameter of testes 0.33 and 0.39; ova 0.11 and 
0.07 in the two principle diameters.” 

Looss (1907 :613-14) criticizes Stafford for establishing a genus without 
description. As Looss shows, the trematode seems to agree with the genus 
Lepocreadium Stoss. This genus was established in 1903, or prior to 
Stafford’s Homalometron. 

The genus Lepocreadium contains the following species: JL. album 
(Stoss.), L. pegorchis (Stoss.), L. trulla (Lint.) and L. levinseni (Lint.). 
Odhner (1905) erects a new sub-family of the Allocreadiidae, Lepo- 
creadiinae, for this genus and Lepidapedon (=Lepodora). In a later paper 
(1914) Odhner identifies the cercaria of Lepocreadium album, the type 
species, and gives an account of the morphology of the adult. As is common, 
some of the most distinctive characters of the genus are found in the distal 
male genital apparatus. 

The present form is strikingly like the genus Lepocreadium. It shows 
similar size, form, spiny cuticula, suckers, digestive system, excretory 


213] SOME NORTH AMERICAN FISH TREMATODES—MANTER 87 


system, vitellaria, and position of the gonads. So far as the description of 
Linton shows, the form could easily belong to this genus, the chief point 
of difference being the median location of the genital pore instead of a 
position to the left, as in Lepocreadium. This pore was clearly median also 
in my material. 

The most important features were found in the male reproductive 
apparatus. In Lepocreadium a prominent cirrus sac is present. It encloses 
the prostate gland and an anterior region of the seminal vesicle, which is 
thus divided into two parts. In the form from Fundulus, however, the 
cirrus sac is entirely absent. The seminal vesicle is globular and swollen 
in form and is not divided into two regions (Fig. 55). It opens directly into 
the pars prostatica, the glandular cells of which lie free in the parenchyma 
at about the level of the ventral sucker. The prostate gland is poorly 
developed. The vagina seems to join the male duct shortly beyond the 
prostate gland and there is a long genital sinus. The absence of a cirrus sac 
would seem to be of generic significance and, in fact, together with the 
median genital pore, violates the sub-family diagnosis. Other features of 
the trematode are so similar to Lepocreadium that it must be considered 
a very closely related genus. 

The seminal receptacle is large and located close behind the seminal 
vesicle, as in Lepocreadium. A short Laurer’s canal is present. No spines 
could be detected in the cirrus or vagina. The yolk reservoir is large and 
located posterior to the ovary. The eggs are very large. A specimen with 
only two eggs showed them to be fully as large or even larger than the 
ovary. The spiny or scaly cuticula layer is very evanescent as has been 
noted for Lepocreadium, and may be lost in preserved material. It is most 
conspicuous on the dorsal anterior regions and thins out in the tail region. 
The glandular mass about the posterior tip of the excretory vesicle is 
present as in Lepocreadium. 

Very young forms of this distome were sometimes found in large 
numbers embedded in the intestinal folds of the host. Moreover, from the 
stomach of the fish cysts were found which clearly contained this trematode 
as shown by the finely spined cuticula of the cercariae within the cysts. 
As the Fundulus had been in salt water aquaria for some time, the indica- 
tion is that infection is derived from marine rather than from fresh water 
sources. In spite of the fact that immature specimens were sometimes found 
in large numbers, infection with the adult form was never heavy, and many 
uninfected fish were found. Usually not more than two or three specimens 
were taken from one host. 


88 ILLINOIS BIOLOGICAL MONOGRAPHS [216 


STEGANODERMA FORMOSUM STAFFORD 1904 
[Figs. 58-60] 
From pyloric ceca, Hippoglossus hippoglossus (Halibut) 


Six specimens of this interesting trematode were obtained from the 
ceca of a single halibut. The only description of the form seems to be by 
Stafford who also found it in the ceca and intestine of the halibut. 

The taxonomic position of this trematode is very close to the genus 
Lecithostaphylus Odhner 1911 (Odhner 1911a) which it markedly re- 
sembles, but from which it differs in certain distinct characters. The genus 
Lecithostaphylus is placed by Odhner in the family Zoogonidae, and, 
indeed, is used as a basis for a new sub-family, Lecithostaphylinae. In- 
cluding the present genus, the family contains the following genera: 

Family: Zoogonidae 
Sub-family: Lecithostaphylinae 
Genus: Lecithostaphylus 
Steganoderma 
Proctophantastes 
Lepidophyllum 
Sub-family: Zoogoninae 
Genus: Diphterostomum 
Zoogonoides 
Zoonogenus 
Zoogonus 


Odhner places Lecithostaphylus ‘‘an die Spitze der Familie” and from 
this genus assumes that the entire family might be derived from the, 
Fellodistominae (Steringophorinae of Odhner*) with which it agrees in 
genital and digestive systems. In the Fellodistomidae, the cirrus is short 
and wide, a condition occurring also in Lecithostaphylus but differing 
from its elongate form in the remaining genera of the Zoogonidae. Stegano- 
derma combines the elongate cirrus with marked similarities to Lecitho- 
staphylus, and hence represents a step between the latter and other genera 
of the sub-family. 

An outline of the genus based on Stafford’s description with some 
additions might be as follows: Body elongate, regular in outline, flattened, 
both ends regularly rounded, anterior end slightly broader. Scale-like 
spines covering body to near the posterior end. Suckers about equal in 
size, ventral sucker a little more than 1/3 from the anterior end. Very 
small pharynx, long esophagus, ceca extending slightly more than half 
the body length. Ovary median or to one side, just posterior to the ventral 
sucker. Testes side by side at ends of ceca. Uterus between testes and 
filling posterior body. Cirrus sac somewhat elongate, almost straight, 


* Nicoll (1913) is correct in pointing out that Odhner is not justified in changing Fello- 
distominae Nicoll to Steringophorinae. 


215) SOME NORTH AMERICAN FISH TREMATODES—MANTER 89 


reaching posteriorly to and sometimes overlapping the ventral sucker, 
crossing left cecum between ventral sucker and the forking of the intestine. 
Genital opening ventral and to the left about half way between cecum and 
margin of body. Vitellaria lateral, reaching only from ventral sucker to 
the testes, composed of a few large follicles. Laurer’s canal present. Type 
species: S. formosum Stafford. 

This genus is like Lecithostaphylus Odhn. in body shape, size, spiny 
cuticula, intestine, gonads, vitellaria, and uterus; but differs from it in 
possessing a very small pharynx, long esophagus, elongate cirrus, well 
developed excretory bladder, and Laurer’s canal with pore. 

The following measurements are from an average sized specimen: 


Men pthread s Guasave sxerenis.s.ssebeerayele traesvenac 3.25 mm. 
SW ih Chae co asec at Sis ciate siare ese gers akonoreatew:srasisorastians 0.86 
PEDIGENESS jcc aie cletsfeisiians aact aces vance 0.2 to 0.28 
Oral Suckenics.sccissalecieucawierls. ocieraveves evecare 0.224 
Ventralistckers) (ern cdtenesnetis cee cdc 0.24 
Diameter of ovary.............0ecceeeeeee 0.26 
Diameter: of tésteSis.cgese ccs a aden seats wee 0.355 
(pharynx ve ernie erste ain ee aicctevois oe Ma hia rsteeers 97 by 68u 
Psophagusicsssacc can + sieamieces qaseesa,. 0.285 

I goSiyoc te cie tetas cciticnmsticieeesemedresant 34 by 17u 


There is no pre-pharynx. The posterior end of the esophagus splits 
into two short branches each about 46u long. That is, the intestine proper 
does not begin at the point of bifurcation, but the esophagus histologically 
extends slightly beyond this point. 

The excretory system is simple, expanded tube-like in form, and extends 
from the posterior tip almost to the posterior border of the ventral sucker 
where it spreads out laterally, T-like. It lies mostly dorsal to the uterus. 
Near its anterior end it becomes so swollen as to fill the larger part of a 
cross-section of the body in that region. It here comes in close contact 
with the intestinal ceca from which it is separated by a very narrow 
distance (Fig. 59). An excretory duct at the posterior tip of the vesicle is 
lined by a cuticula-like layer continuous with the external body cuticula. 
In the parenchyma about this duct appear what seem to be gland cells, 
pyriform in shape and with large nuclei (Fig. 60). 

Within the parenchyma, in the anterior body region, especially in the 
vicinity of the esophagus, numerous, conspicuous, round to oval bodies 
occur. They are without nuclei and their content is very finely granular 
and homogeneous. They exhibit a very strong affinity for eosin stain, 
which colors them immediately and tenaciously. These bodies which 
almost fill the parenchyma anteriorly thin out posteriorly, and disappear 
at about the level of the ventral sucker. Their size varies, being about 
13 to 39y in longest diameter. The nature and function of these bodies 
could not be determined. They were not found in any other trematode 


90 ILLINOIS BIOLOGICAL MONOGRAPHS [216 


of the present collection. The cells in the neck region of Siphodera de- 
scribed by Linton (1911) differ markedly from these bodies in appearance. 
In Siphodera, the cells have definite nuclei. 

The position of the ovary is just posterior to the ventral sucker, but it 
may be either median or slightly to one side. The ootype is small, without 
membrane, and lies posterior to the ovary. Laurer’s canal is present, is 
only slightly coiled, and opens dorsally just posterior to the ovary. A sem- 
inal receptacle seems to be absent. The uterus leads posteriorly, coiling 
between the testes, filling the hind body, and returning to course ventrally 
over the ovary. The vagina begins at about the level of the ventral sucker, 
leads anteriorly and obliquely to the left parallel with the cirrus sac, to 
which it is at first lateral on the left and then dorsal. The male duct joins 
the vagina ventrally and there is a common genital sinus for a short distance 
about 60x. 

The number of follicles in the vitellaria is fairly but not exactly 
constant. It is sometimes difficult to determine the exact number, as some 
follicles are seen to be double in nature, an indication of an evolutionary 
change either toward a more compact or a more diffuse condition of these 
organs. Eight or nine follicles were found on the right side and ten to twelve 
on the left. 

The two ducts from the testes arise from the anterior aspects of these 
organs and course anteriorly lateral to the excretory vesicle and between 
this organ and the ceca. The ducts unite just posterior to the termination 
of the excretory vesicle, and continue forward for some distance as a single 
duct in the mid-body region. At about the level of the anterior border of 
the ventral sucker this duct enters the muscular cirrus sac and becomes 
the seminal vesicle. This vesicle is poorly developed. It is scarcely, if any, 
coiled. A slight constriction separates it from the well-developed pars 
prostatica which, surrounded by gland cells, occupies most of the cirrus 
sac. The ejaculatory duct is unarmed. In the 3.25 mm. specimen the 
cirrus sac measured about 0.69 mm. in length and 0.19 mm. in width at 
its widest point. The seminal vesicle extended about 0.176 mm., the pars 
prostatica 0.34 mm., and the ejaculatory duct 0.17 mm. 


THE HEMIURIDAE 


The Hemiuridae include many of the most common marine trematodes. 
Typical members of the family are those forms with a “‘tail appendage”’ 
such as Hemiurus, Brachyphallus, and Dinurus. Liihe founded the family 
in 1901, and included in it also such forms as Derogenes and Accacoelium. 
Looss (1907a) later limited the conception of the family, excluding the two 
latter genera. Odhner (1911b) points out that Derogenes is so closely 
related to the other Hemiuridae that separation from that family is 
impossible. The inclusion of Derogenes necessitates the adoption of 


217] SOME NORTH AMERICAN FISH TREMATODES—MANTER 91 


Genarches and other Syncoeliinae. Odhner also included the Accacoeliinae 
and the Hirudinella clavata group. Nicoll reviews the status of the family 
and agrees with Odhner in accepting its broader conception according 
to which ‘“‘Looss’s Hemiuridae takes the position of a sub-family”’ (Nicoll 
1913:245). Nicoll also extends the boundaries of the family slightly to 
include his genera, Hemipera and Derogenoides. The family has thus 
become so broad as to be very difficult to describe. At present, it must be 
considered as a large variable group, containing (Nicoll 1915) the following 
sub-families: Hemiurinae, Diurinae, Sterrhurinae, Lecithasterinae, 
Syncoeliinae, and Accacoeliinae. Considering Hirudinella as belonging in 
the last sub-family, members of each of these sub-families except Dinurinae 
have been met with in the present studies. 

A few words should be said in respect to the use of the term ‘‘cirrus 
sac” in this group (Hemiuridae). In the Hemiuridae, the two sex ducts 
unite to form a more or less elongate tube-like ‘‘ductus hermaphroditus”’ 
or genital sinus which leads to the common genital pore. This condition 
of the terminal genital region in the Hemiruidae has been rather fully 
discussed in the literature. Pratt (1898) reviews the situation and gives 
its history to 1898. Levinsen (1881) and Juel (1889) termed the common 
terminal portion of the genital tract the genital vestibule. It is perhaps 
now more commonly known as the genital sinus. Pratt and Juel both 
believe that the terminal portion of this vestibule or genital sinus has 
arisen as ‘“‘an invagination of the body wall and is homologous to the 
genital cloaca of other trematodes.”’ Juel believes that the remainder of 
the duct represents the distal end of the uterus which has come to serve 
as a genital sinus by the dropping back of the ejaculatory duct. Pratt, 
however, believes that it has been the uterus that has dropped back and 
hence that most of the sinus is homologous with the forward end of the 
ejaculatory duct. 

Whatever its origin, it is known that this genital sinus can function as 
a cirrus, and is protrusible. Looss noted such a functioning in 1896 for 
Apoblema mollissimum. Because the genital sinus functioned as a true 
cirrus, the muscular sac surrounding it he considered as a true cirrus sac. 
He says (p. 125): ‘Or, en ne tenant compte que de ses rapports avec le 
canal renfermé, je crois déja pouvoir la considérer avec raison comme une 
véritable poche du cirrhe: ces fonctions viennent parfaitment a l’appui de 
cette interprétation.”” In the same discussion, however, Looss himself 
notes that the term is not strictly correct. Thus, in regard to “la poche 
du cirrhe,” he says (p. 127): .... “a proprement parler ce terme n’est 
pas tout 4 fait exact; mais Poaiaisaant maintenant ses rapports avec le 
reste des organes génitaux, nous pouvons nous en servir pour plus de 
simplicité.”’ Other authors (e.g., Lithe 1901, Lander 1904, Odhner 1905, 


92 ILLINOIS BIOLOGICAL MONOGRAPHS [218 


Lebour 1908) agree in calling the muscular sac around the genital sinus a 
true cirrus sac. 

Strictly speaking, it does not seem appropriate to refer to this structure 
as a true cirrus sac. The cirrus is a definite organ belonging strictly to the 
male genital system. The genital sinus in Hemiuridae, although functioning 
as a cirrus and although probably homologous with the cirrus, cannot be 
termed a true cirrus, since it is a duct common to both male and female 
systems. It has never been referred to as a cirrus, but as the “‘genital sinus” 
or “ductus hermaphroditus.”” To call the sac surrounding it a cirrus sac is 
then a misnomer. Since this structure surrounds the genital sinus, it seems 
more appropriate to refer to it as a sinus sac. This sinus sac in Hemiuridae 
certainly functions as a cirrus sac, and is probably homologous with the 
cirrus sac. The difference is, however, a distinct one. For the expression 
of the association of the sac with a common sex duct instead of with the 
male duct alone, it is felt that the term “sinus sac’’ is justified. It has 
already been used by the present author in an earlier paper (Manter 1925). 
Some such term seems all the more advisable in view of the fact that in 
Nicoll’s genus Hemipera a true cirrus sac appears to be present, containing 
‘not only the ductus ejaculatorius but also the pars prostatica” (Nicoll 
1913:245). 


HEMIURUS LEVINSENI ODHNER 1905 
[Figs. 62-63] 


From stomach, Gadus callarias (Cod) 
From stomach, Urophycis chuss (Squirrel hake) 


Species of the genus Hemiurus are among the most common trematodes 
of marine fish. Distinction between species is, however, rather difficult. 
Looss in 1907 perhaps drew the most careful lines between species. It has 
been customary, especially previous to 1907, to refer most specimens which 
are clearly Hemiurus to the species appendiculatus. Thus, Stafford (1904) 
lists H. appendiculatus from ten different fish of Canadian waters. His 
only comment is: ‘Suckers of equal size.’’? Looss shows that true H. appen- 
diculatus up to 1907 had probably been found only in Alosa finta. He adds 
the additional hosts, Gadus euxinus and Mugil capito, in the latter of which 
the parasite might be accidental. 

The following are some of the most distinctive characters of H. ap- 
pendiculatus as given by Looss: Ventral sucker about twice as large as 
oral sucker; ringing of the cuticula disappearing dorsally at about the level 
of the pharynx; cirrus sac elongate, reaching a length about 3/4 the 
diameter of the ventral sucker; anterior part of the seminal vesicle very 
muscular; coils of uterus can stretch relatively far into the tail appendage, 
and come near the ends of the ceca. 


219] SOME NORTH AMERICAN FISH TREMATODES—MANTER 93 


All of the material collected from the Mount Desert Island region and 
belonging to the genus Hemiurus apparently belongs to the species, 
H. levinseni. The almost equal size of the suckers, with the oral sucker 
slightly larger is a constant character and one which separates the species 
from H. appendicualtus, H. communis, H. liihei, and H. rugosus. Since all 
of Stafford’s representatives of this genus collected from Canadian fish 
show this character, it is very probable that they should belong in this 
species rather than in H. appendiculatus. Odhner reports H. levinseni from 
Gadus morrhua {, ovak, Cottus scorpius, and ‘‘many northern fish.” It 
seems to be the most common Hemiurus species in arctic marine fish. In 
temperate waters the other species showing larger ventral suckers and 
small oral suckers are common. Thus, Linton’s Dist. appendiculatum from 
Woods Hole fish shows a sucker proportion of about 1 : 2. 

Hemiurus levinseni also differs from H. appendiculatus in possessing a 
shorter prostate tube, in a more constantly retracted tail appendage into 
which the uterus does not commonly extend, and in the cuticular rings 
extending dorsally to the level of the ovary. 

In the present material, as in Odhner’s, the tail was almost always 
completely retracted. The ceca may enter the tail slightly. In a single 
specimen the tail was fully extended and in this case both the ceca and a 
portion of the uterus extended into it (Fig. 62). The genital pore is median 
just behind the mouth opening. The genital sinus is long, and in contracted 
specimens the prostate tube does not begin until about the level of the 
ventral sucker. This tube is long and more or less curved according to 
body contraction. ‘The seminal vesicle is large and divided into two 
sections, the anterior of which is surrounded by a muscular coat. The sizes 
of the specimens vary from 0.7 mm. to 1.68 mm. in length. Eggs measure- 
ments of 23 to 26 by 10 to i3u agree well with Odhner’s measurements of 
26 to 28 by 12 to 13y. 

Eighteen specimens were taken altogether from the stomachs of six 
squirrel hake examined. Eight specimens were collected from three cod. 

Cooper (1915) reports this species encysted in the muscles of small 
herring. 

Measurements on four typical specimens are as follows: 


Men gt ire corsvevisiesv s.cvens 1.68 mm. 1.12 mm. 1.06 mm, 0.99 mm. 
Widths s,ero.siecece.csstec's 0.467 0.37 0.374 0.37 

Oral sucker..<...0.0026 0.176 0.176 0.142 0.159 
Ventral sucker........ 0.188 0.17 0.136 0.142 
PhALyNK i 2 oc .civisis.e a a 91 by 91p 91 by 74u 68 by 624 85 by 74p 


ESOS iecccereia eress-s sores sae 2312p 2313p 26 10-13 p 


94 ILLINOIS BIOLOGICAL MONOGRAPHS [220 


BRACHYPHALLUS CRENATUS (RUDOLPHI 1802) 
[Fig. 53] 
From stomach and intestine, Osmerus mordax (smelt) 
ba « ¢ Pollachias virens (Pollack) 
€ © «& g Clupea harengus (Herring) 

Lander (1904) has described the morphology of this form in detail. 
His material was also obtained from the smelt. In the present collection 
thirteen specimens were obtained from the stomachs and intestines of 
three smelt. Two other fish examined did not contain the trematode. 
The worms usually occur in the stomach. 

Looss (1907:158) expresses the view that the American form of this 
parasite represents a new species which he names B. affinis. He finds the 
chief distinction to be the elongate and less lobed condition of the vitellaria 
and that the host and geographical occurrence differ widely from the 
European B. crenatus from Salmo salar. Lander figures the vitellaria as 
about twice as long as wide in an extended specimen, and his description 
indicates that this is the usual condition. In regard to lobation of these 
organs, Lander says: ‘‘They are commonly slightly lobulated, though they 
sometimes have a regular oval outline.”” Cooper (1915) describes and 
figures one specimen from a small herring. This specimen agreed with 
B. crenatus in having definitely lobed vitellaria (right, four lobed; left, 
three lobed). He also points out that either gland may appear entire when 
viewed obliquely. He suggests that the herring may represent an inter- 
mediate host and that the trematode might be discovered in Salmo salar 
from America. 

The present material from the smelt agrees with descriptions of B. 
crenatus (Rud.). It is probably the same species collected by Lander from 
the same host. The vitellaria, however, in my specimens from the smelt 
were always distinctly lobed (Fig. 53), usually one being four-lobed, the 
other three-lobed. In none of the specimens were the vitellaria noticeably 
longer than wide. On the basis of these thirteen specimens from the smelt, 
it would appear that the American species is not distinguishable from the 
European species, B. crenatus. For hosts of Brachyphallus crenatus Odhner 
gives: Cottus scorpius, Pleuronectes limanda, Gasterosteus aculeatus, 
Ammodytes tobianus, Salmo salar and trutta, and Osmerus eperlanus. 
Lander’s material was from Osmerus mordax and Anguilla chrysypa. 

The smelt from which the present material was collected occurred in 
large numbers, together with small cod and pollack beneath the fishing 
wharf at Manset. All these fish were about the same size and evidently 
had similar feeding habits. The same trematode, Brachyphallus crenatus, 
was obtained from the stomach of the pollack, Pollachius virens, but not 
from the cod. Specimens from the pollack agreed in every respect with 


221] SOME NORTH AMERICAN FISH TREMATODES—MANTER 95 


those from the smelt. They were relatively small and usually contracted. 
The vitellaria were constantly lobed. Four fish yielded eleven trematodes. 

Eight or nine specimens were obtained from the examination of 28 
herring (Clupea harengris). The much larger size of most of these trema- 
todes gave the impression of a different species, but the details of anatomy 
agreed with Brachyphallus crenatus. Moreover, the sizes agree with known 
limits for the species (Odhner recording a variation of 0.8 mm. to 2.5 mm. 
in body length, while Olsson gives 5 mm. as maximum length). Cooper 
(1915) found one small specimen in the stomach of the herring. The 
present collection of large mature specimens from this host indicates that 
the herring is a normal host for the parasite and not, at least exclusively, 
an intermediate host as suggested by Cooper. 

Only in material from the herring was variation in vitellaria shape 
noted. In these specimens, lobing of the vitellaria was not common. The 
characteristic four- and three-lobed condition was clearly evident, how- 
ever, in one specimen. The material from the herring agrees in this respect 
with Lander’s description, although an elongate condition of the vitellaria 
was not common. 


LECITHASTER GIBBOSUS (RUDOLPHI 1802) 
[Fig. 61] 
From intestine, Myxocephalus octodecimspinosus (2), Sculpin 


Looss (1907) gives the following synonyms for this species: 


Distomum mollissimum Lev. 1881! 
nec Distomum mollissimum Stoss. 1889 
nec A poblema mollissimum Lss. 1896 


Odhner (1905) reports this species from various northern fish (including 
Cottus scorpius). He separates the species from Lecithaster confusus Odhner. 
This latter species has the following synonymy: 


A poblema mollissimum Lss. 1896 
nec Distomum mollissimum Lev. 1881 

Hemiurus bothryophorus Lss. 1899 
nec Distomum botryophoron® Olss. 1868° 


A single specimen was collected from the intestine of one fish out of 
eleven examined. Stafford (1904) reports a species as Lecithaster bothryo- 
phorus Olsson (=A poblema mollissimum) from the salmon and herring. 


1 This date printed 1891 was evidently a misprint. 

2 Olsson originally spelled this name botryophoron, but the word has been very commonly 
referred to as bothryophoron. Liihe (1901) called the species Lecithaster bothryophoron using 
it as type of the genus Lecithaster. Odhner (1905) shows this species to be actually Lecith- 
aster gibbosus (Rud.). 

3 Given as 1869, 


96 ILLINOIS BIOLOGICAL MONOGRAPHS [222 


Odhner (1905) assigned Lecithaster bothryophorus as the type of a new 
genus Lecithophyllum. As Apoblema mollissimum is a synonym of 
Lecithaster nfusus, the actual identification of Stafford’s material which 
is undescribed is unknown. Linton (1901 and 1905) reports Dist. bothryo- 
phoron from various fish, but to which species of Lecithaster his form 
belongs cannot be determined from his descriptions or figures. 

The two species Lec. confusus and Lec. gibbosus are closely related. 
The present specimen was assigned to the latter species because of the 
thickness of the ovarian lobes, the length of the vitelline lobes, and because 
the seminal vesicle did not extend posterior to the ventral sucker. Accord- 
ing to Looss, these three points are the chief means of distinction between 
the two species. 

Measurements on the specimen are as follows: 


Deen gti dere ctec.c seelele cetesisteis aitvenarsteaieane ereieie 1.12 mm. 
Width 25.) cg. ca eee aan ea ee ene e 0.4 

Oral sucker: 22 crave crowitdueern caleweronnteneit 0.17 
Ventral suckers 20. -ycecitecreeiee ee eit 0.256 
Pharynx sr. s csrsitn o-warerorecrrsarnervons +s 0.09 by 0.09 
POSES oa. cs.asatacs opcayacardaleterajaieavs aceiaese ses 23 to 26 by 15h 


APONURUS SPHAEROLECITHUS MANTER 1925 
[Figs. 70-74] 
From stomach, Urophycis tenuis (Hake) 


The genus Aponurus is considered by Looss (1907) as most nearly 
related to Lecithaster, although showing relationships to Brachyphallus. 
The only other species in the genus is A. laguncula Lss. 

The trematodes of this genus are small in size (about one millimeter 
in length) and almost cylindrical in form, tapering anteriorly but broadly 
rounded posteriorly. The ventral sucker, located about 1/ 3 from the 
anterior end, is almost exactly twice the size of the oral sucker. The 
genital pore is about at the level of the pharynx. The genital sinus is 
surrounded by a conspicuous pear-shaped sinus sac. Vagina or metraterm 
is lacking or very short. Seminal vesicle rather short, swollen, mostly 
anterior to the ventral sucker. Testes, ovary, and vitellaria globular. The 
vitellaria are in two groups, one of four, another of three follicles. They 
are more or less spherical, and are located just posterior to the ovary. 
Coils of the uterus fill the body posterior to the vitellaria, but anterior to 
the ovary are more limited to the space between the intestinal ceca. 

The genus Aponurus bears close relationship to Lecithaster and 
Lecithophyllum. Lecithophyllum was created by Odhner (1905) for 
Olsson’s Distoma botryophoron. Odhner studied Olsson’s type material. 
The following table, showing differences between the three genera is based 
on data as given by Odhner and Looss. 


223] 


Lecithaster 
(1) Genital pore rather distant 
from oral sucker 
(2) Ovary 4lobed 
(3) Posterior end tapering 


(4) Pars prostatica much longer 
than genital sinus 

(5) Genital sinus reaching about 
to ventral sucker 


(6) Eggs small (15 to 254) thin- 
shelled 

(7) Vitellaria elongate in 7 con- 
nected parts 


SOME NORTH AMERICAN FISH TREMATODES—MANTER 


Lecithophyllum 
Genital pore rather close to 
oral sucker 
Ovary entire 
Posterior 
rounded 
Pars prostatica shorter than 
genital sinus 
Genital sinus reaching al- 
most to ventral sucker 


end _ broadly 


Eggs large (60u)  thick- 
shelled 

Vitellaria elongate in 7 con- 
nected parts 


97 


A ponurus 
Genital pore rather close to 
oral sucker 
Ovary entire 
Posterior 
rounded 
Pars prostatic as long as 
genital sinus 
Genital sinus reaching only 
about half way to ventral 
sucker 
Eggs small (26x) 


end _ broadly 


Vitellaria rounded in 7 
separate parts 


The significance to be attached to the distinctly separated nature of 
the follicles of the vitellaria might be questioned and perhaps should not 
be considered as of generic value. Looss himself brings up this question. 
In his discussion of Lecithaster he says (Looss 1907:161): ‘“‘Einen gewissen 
Anklang an die bei den Verwandten herrschenden Verhiltnisse kann man 
vielleicht darin erblichen, dass die 7 Schlauche nicht selten so gelagert 
sind, dass mehr oder weniger deutlich eine Gruppe von 4 und eine von 3 
Schléuchen ensteht.”” Yet in Lecithaster and Lecithophyllum the follicles 
are described as distinctly united centrally. Again, Looss seems to express 
some doubt as to whether the vitellaria in Aponurus are all actually un- 
connected. He says (p. 168): ‘‘Bei der Pressung frischer Tiere geht die 
Kugel-form in eine Birn- oder Keulenform iiber, die Gruppen von 3 und 
4 bleiben meist deutlich sichtbar, verschinden manchmal aber ebenfalls, 
und dann dhneln die Dotterstécke vollkommen denen von Lecithaster, 
da die Schlauche alle von einem Punkt auszugehen scheinen. Ich glaube 
auch, dass dies tatsichlich der Fall ist, obwohl der direkte Nachweis an 
ganzen und aufgehellten Individuen wegen der ungiinstigen Lagerung der 
Follikel nicht zu erbringen ist.’’ Yet, if it be true that the vitellaria are 
actually as in Lecithaster then there is much less justification for separation 
of Aponurus from Lecithophyllum. The condition of the vitellaria in the 
present material will be discussed below. 

Two specimens of this form were obtained from the stomach of one 
fish. These specimens agree in the main with the characters of the genus. 
Both seemed fully mature and their size measurements were 1.47 by 
0.29 mm., and 1.1 by 0.245 mm. The greatest thickness is about the same 
as the greatest width, so that at the ventral sucker and posterior the worm 
is cylindrical. The body is broadly rounded at the posterior end. The 
cuticula is smooth and there is no tail appendage. The sucker proportion 
is almost exactly 1:2. Pre-pharynx lacking, pharynx globular; esophagus 
short; wide ceca reaching to the posterior end of the body. 


98 ILLINOIS BIOLOGICAL MONOGRAPHS [224 


The excretory system is as in other Hemiurids. Posteriorly it is con- 
cealed by egg masses. The unpaired vesicle branches between the ovary 
and testes, and the two lateral branches unite dorsal to the pharynx. 

The genital pore is ventral, median, at about the level of the middle of 
the pharynx. The pear-shaped muscular sinus-sac extends dorsally and 
posteriorly from the pore and surrounds the genital sinus. It reaches about 
half way to the ventral sucker. In this posterior extent of the genital sinus 
the form differs from Lecithophyllum. The wall of the sac consists of an 
outer layer of longitudinal muscles and an inner layer of circular muscles. 
Between these layers and the sex duct is a space filled by parenchyma 
tissue containing a few cells. The width of this parenchyma-filled space is 
about.equal to the combined thickness of the muscle layers. The common 
genital duct coils somewhat within the sac, at the posterior end of which 
it splits into the male and female sex ducts. 

The testes are located a short distance posterior to the ventral sucker. 
In both specimens the right testis was slightly anterior to the left. Their 
size is relatively small, and in this respect they differ from the condition in 
A. laguncula, where the testes fill a large portion of the body cross-section. 
The seminal vesicle is large, and ovoid or simple-sac like in shape. In 
A. laguncula it is bent slightly at each end. In the present species it extends 
posteriorly to near the middle of the ventral sucker. In A. laguncula, it 
does not extend very far beyond the anterior margin of the sucker. 

The duct of the pars prostatica leads from the ventral surface of the 
seminal vesicle near its anterior end, bends directly dorsally over the 
anterior end of the vesicle, reaches to the dorsal wall, and then bends again 
ventrally to unite immediately with the uterus to form the genital sinus. 
The wall of the duct is composed of small flat cells apparently without 
ciliary processes. The form of the pars prostatica is S-shaped in lateral 
view (Fig. 70), and the gland does not run directly posteriorly as in A. 
laguncula. The cells of the prostate gland are large in size and somewhat 
angular in shape. The total length of the gland is just about equal to the 
length of the sinus sac. Thus, in length it agrees with A. laguncula and 
differs from Lecithophyllum botryophoron. In a 2 mm. specimen of the 
latter species, the genital sinus was 0.3 mm. long and the pars prostatica 
0.17 mm. or about 1/2 as long. In the 1.1 mm. specimen of A. sphaero- 
lecithus the pars prostatica was about 0.19 mm. in length. In this same 
specimen the sinus sac was about 0.2 mm. in length measured from the 
lateral aspect. This proportional length is about as in Lecithophyllum, 
but due to the dorsal slant of the organ its posterior edge only reached a 
point about half way to the ventral sucker. 

The ovary is located a short distance posterior to the testes and slightly 
to the right. It is spherical in form and smooth in outline. The globular 


225) SOME NORTH AMERICAN FISH TREMATODES—MANTER 99 


seminal vesicle is located anterior and slightly dorsal to the ovary. It is 
about one half the size of the ovary. Laurer’s canal is absent. 

The vitellaria consist of seven follicles, globular in shape a smooth with 
outline, and located close together just posterior to the ovary. They are in 
two groups. One group of four is located to the right and just posterior to 
the ovary, while the group of three is located to the left (Figs. 73-74). The 
follicles in the group of four are larger, being almost as large as the ovary. 
This size of the follicles is greater than in A. Jaguncula, where they are 
about one half the size of the ovary. The position of both ovary and 
vitellaria is near the ventral surface of the body. In regard to the separate 
or connected condition of the follicles, a series of sections through the larger 
specimen gave no indication that the follicles are united at any point. While 
some were in close contact with each other, others were clearly isolated. 
In spite of Looss’s question, this condition seems definitely distinct, 
certainly from the normal condition in Lecithaster and from the condition 
described for Lecithophyllum. More material will be necessary to settle 
the point finally. 

The coils of the uterus are as in A. laguncula. The terminal region of 
the uterus is surrounded by the cells of the prostate gland. The uterus 
runs close to the male duct in this region and with it swings dorsally over 
the anterior end of the seminal vesicle (Fig. 72). The male and female 
ducts do not unite outside the sinus sac. The male duct opens into the 
extreme posterior tip of the sac, while the female duct enters from the left 
at practically the same spot. 

The eggs are very large and this character forms a conspicuous differ- 
ence between the two species of Aponurus. Looss gives the eggs of A. lagun- 
cula as about 0.027 mm. in length and 0.016 mm. in width. Eggs in the 
present species were 0.056 to 0.065 mm. by about 0.026 mm. This size 
and the thick egg shell agree with Lecithophyllum. 

Measurements are as follows: 


Tengthirnaa he Seeration fe terest odiorarn 6 1.47 mm. 1.1 mm. 
WWidth'4. 2. Ser eae ee cweeeeencaieye ae 0.296 0.245 
Oralisuckerss2.0.2i eae se ness 0.137 0.1 
Ventral sucker..................000 0.264 0.19 

Ant. end to post. edge ventralsucker.... 0.617 0.43 
Pharyiax sctaae Meve tacetstotsce civilians melepaceien’ 63 by 63u 57 by 57u 
Diameter, ant. testis................. 68u 57u 
Diameter, post. testis................ 79u 68u 
Diameter, ovary.............-.+-0-- 91u 85yu 
Diameter, vitellaria.................. 85 to 91u 62 to 72u 


Pgs ee ls goa ad 58-62 by 264 56-65 by 26u 


100 ILLINOIS BIOLOGICAL MONOGRAPHS [226 


GENOLINEA LATICAUDA MANTER 1925 
[Figs. 64-66] 
From stomach, Hippoglossus hippoglossus (Halibut) 


Small to medium-sized forms, with flattened body tapering slightly 
anteriorly, at which end it is roundly pointed; body broadly rounded 
posteriorly. Body almost uniformly wide. Cuticula smooth. Tail ap- 
pendage lacking. Oral sucker embedded in body, overlapped dorsally by 
fleshy lip. Ventral sucker about one and a half times the size of the oral 
sucker, located anterior to the middle of the body and about at the end 
of the first body third. No pre-pharynx, pharynx broad, esophagus very 
short, ceca broad, extending to posterior tip of body. Excretory system as 
in Hemiuridae, branches uniting dorsal to pharynx. Genital pore median, 
ventral, at about the level of the forking of the intestine. Testes compact, 
globular, obliquely behind one another some distance behind the ventral 
sucker. Ovary large, compact, globular, located behind testes. Vitellaria 
behind one another posterior to ovary, compact, globular. Uterus sends 
two lateral coils posterior to vitellaria to near body tip. Between ovary 
and ventral sucker the uterus is in large transverse coils. Genital sinus 
short, seminal vesicle much coiled, just anterior or slightly overlapping the 
ventral sucker. Eggs 28 to 31 by 12 to 15y. 

The Hemiurid affinities of this form are seen in the digestive and 
excretory systems, the general form, shape, and position of the gonads, 
the genital sinus, prostate gland, and oral lip. It is most closely related to 
Genarches Lss. and Derogenes Liithe. which are grouped under the Syn- 
coelinae. It differs from both in body shape which is not markedly tapering 
at either end, and in position and proportional size of the ventral sucker 
which is distinctly anterior to mid-body. None of the three specimens 
showed contraction of the neck region, so that this sucker position can 
be assumed as normal. The course of the uterus in Genolinea is distinctly 
different than it is in either Genarches or Derogenes. Genarches is, of 
course, also clearly separated by the union of the two intestinal ceca 
posteriorly. 

Genolinea, in addition to points already mentioned, is distinct from 
Derogenes in possessing a very short prostate gland, a much coiled seminal 
vesicle, and a more linear arrangement of the reproductive organs. 

Measurements on two of the specimens are as follows: 


Eength een eee ene 1.87 mm. 1.32 mm. 
Widthisice occ Satie oa sca o eee 0.336 0.299 
Oral sucker.................00.2000% 0.136 0.125 
Ventral sucker...................... 0.239 0.199 
Ant. end to post. edge ventral sucker... . 0.617 0.5 
Pharynx. ane eco eee 57 by 79u 57 by 74u 


ANCS teStisy sei ace cass ee ene ae neous 0.136 mm. 0.1 mm. 


227] SOME NORTH AMERICAN FISH TREMATODES—MANTER 101 


POSES LESUISI ts ne siere. cicisis-suslaehareysiecs oss 0.136 0.13 
Ova typrtetere yas says ses -tirepaisre, eres suai 0.165 0.15 
Ante vitellariumy i ecte-< assis, cree @ aaa 0.114 O42 
Postavitellanum: .c.52 cies Ace cee one 0.142 0.12 
OB oes Brew apet-avcv ery Vove eh eup ists cwcepearesvarate arses < 31 by 13 to 154 28 to 31 by 12p 


GONOCERCA PHYCIDIS MANTER 1925 
[Figs. 67-69] 
From gills and branchial cavity, Urophycis chuss (Squirrel Hake) 


Body elongate, both ends bluntly rounded, cuticula smooth, not ringed, 
body only slightly flattened, oval in cross-section, tail appendage lacking. 
Ventral sucker posterior to middle of body, almost twice as large as the 
oral sucker, about as wide as body. Mouth opening sub-terminal, over- 
lapped dorsally by lip-like projection of body, oral sucker embedded in 
body. No pre-pharynx, short esophagus, intestinal ceca reaching to 
posterior end of body. Excretory vesicle branching just posterior to the 
ovary, the branches running forward laterally and uniting dorsal to the 
oral sucker near the anterior tip. Gonads crowded together posterior to 
the ventral sucker and filling most of the body space in that region. Genital 
aperture median and ventral, close behind mouth opening. Ovary median 
just behind ventral sucker, anterior to the testes. Vitellaria compact, un- 
lobed, lateral and very slightly posterior to the ovary. Testes large, just 
posterior to the ovary, obliquely behind and in contact with each other. 
Ootype without membrane, dorsal and anterior to the ovary. Eggs com- 
paratively large. Seminal vesicle comma-shaped, pointed anteriorly, 
located at about the level of the pharynx. Prostate gland little developed, 
free, short, located ventral to the oral sucker just anterior to the seminal 
vesicle. The covering of the seminal vesicle seems to be non-muscular, 
hence the cirrus sac is absent or at most weakly developed. There is a 
short genital sinus. No localized seminal receptacle. Region of the uterus 
just anterior to the ovary often crowded with sperm cells. 

About 15 specimens were taken from the gills and branchial cavity of 
a single host. The fish had been caught but a few hours and it is possible 
that (as is true of some other Hemiurids) the gill region is the normal 
habitat of the parasite. Two specimens altogether, however, were obtained 
from the stomach of this fish. 

That this trematode belongs to the non-appendiculate Hemiuridae 
there can be no doubt. Its features characteristic of the family are seen’ 
in the excretory system, projection of upper lip, position of genital pore, 
and character and form of the gonads. It differs from most members of 
the family in the reversed position of the ovary in relation to the testes. 
Still more marked distinctions are found in the location of the uterus 
entirely anterior to the ovary, in the position of the seminal vesicle far 


102 ILLINOIS BIOLOGICAL MONOGRAPHS (228 
distant from the ventral sucker, in the position of the prostate gland, and 
in the crowded localization of the gonads and vitellaria in the tail region. 

The occurrence of the parasite on the gills and in the branchial cavity 
of the host is not unique among the Hemiuridae. Odhner gives the follow- 
ing as “‘gill parasites’: Accacoelium contortum, Syncoelium, Otiotrema, 
Bathycotyle, and Liocerca. Of these forms, the present species resembles 
most closely Liocerca. Liocerca is also one of the few members of the 
family with testes posterior to the ovary. Gonocerca differs markedly, 
however, from Liocerca in the following points: position of the genital 
pore, which is considerably more posterior in Liocerca; position of the 
seminal vesicle, which is close to the ventral sucker in Liocerca; length of 
the prostate gland, which is elongate in Liocerca; and in uterine coils, 
which extend posterior to the ovary in Liocerca. Liocerca shows more 
resemblance to Hemiurus than does Gonocerca. 

Nicoll in 1913 describes the genus Hemipera which he considers most 
closely related to Liocerca. It resembles this genus in inverted position of 
the ovary. In this respect, it is also like the present form with which it 
shows further similarity in position of the ventral sucker. The body form 
of all three genera is very similar. In Hemipera, the testes are lateral to 
each other, instead of behind one another, as in the other two genera. 
Hemipera shows the widest divergence in possessing a cirrus sac inclosing 
both prostate gland and seminal vesicle, and in having egg with polar 
filaments. 

A tabular comparison of these genera follows: 


Liocerca Gonocerca Hemipera 
Habitat gills gills stomach 
Position of genital Somewhat distant Close to oral sucker Somewhat distant 
pore from oral sucker from oral sucker 
Position of ventral About mid-body Posterior to mid- Posterior to mid- 
sucker ~ body body 
Testes Behind one another Behind one another __ Lateral to each other 
Cirrus sac Inclosing only male Absent Inclosing prostate 


duct 


gland and sem. ves. 


Prostate gland Free, elongate Free, short Inclosed 

Seminal vesicle Near ventral sucker Near pharynx Between suckers 

Eggs Numerous, non- Numerous, non-_ Few, filamented 
filamented filamented 


Form, shape, size, cuticula, excretory and digestive systems are similar 


in all three genera. 

Gonocerca differs from Derogenes in extent and position of prostate 
gland, position of genital pore, course of uterus, and inverted position of 
ovary in relation to testes. These same differences except extent of prostate 
gland separate it from Genarches. 


229] SOME NORTH AMERICAN FISH TREMATODES—MANTER 103 


Measurements on five specimens are as follows: 


Wengthies tees secs 1.8 mm. 1.9 mm. 1.3 mm. 1.4 mm. 1.4 mm. 
Widthwaie ores osciee es 0.48 0.37 0.29 0.37 0.4 
Ant. end to post. border 

ventral sucker......... 123 1.3 0.89 1 1. 
Oralsucker............. 0.26 0.22 0.18 0.2 0.22 
Ventralsucker...... : 0.43 0.37 0.29 0.33 0.35 
Ovaryeeacansa: ie oee pe 0e2, 0.12 0.13 0.12 0.125 
WesSteS: coi cess nccteees 0.22 0.19 0.17 0.23 0.23 
Witellaria..o...: 5055... 0.15 0.1 0.1 0.114 0.114 
Pharynxse). sae 114 by 854 80by 80u 74 by 85u 96 by 5p 85 by 79u 
Bees Mee eewaG eras ; 46 to 50 by 20 to 26u 


DEROGENES VARICUS (MULLER 1784) 
. [Fig. 57] 
From Stomach, Gadus callarias (Cod) 
hs o Urophycis tenuis (Hake) 
oe « Urophycis chuss (Squirrel hake) 
& « Anarrhichas lupus (Wolf fish) 
Intestine, Hippoglossus hippoglossus (Halibut) 
& Myxocephalus octodecimspinosus (Sculpin) 

This parasite is known as perhaps the most common marine fish 
trematode. It shows a very extensive host range, although usually present 
in small numbers. Nicoll reports mature specimens as small as one milli- 
meter in length while Stossich gives a maximum length of 7 mm. The 
parasite is quite easily distinguished from other Hemiurids by its lack of 
tail appendage, position of ventral sucker posterior to middle of the body, 
small terminal sinus sac inclosing both sex ducts, its long prostate, and large 
eggs. There is no pre-pharynx. The genital opening is about at the level 
of the branching of the intestine. Gonads are similar to those of the typical 
Hemiurids. Measurements on an average sized specimen from the cod 
were: 


Length........ ee Saisie emia es le mM. 
Width...... RRs Bone tae kOe 

Oral suckers jeune serene eaaeen ascii: 0.22 

Ventral sucker? a csi25.4.y0eae4 nase 0.37 

OWaLY vent gta ates a otea@ eal 0.14 x-diameter 
SRESTES IM ere sxc ots fens ce ateeease ee 0.14 x-diameter 
Phar ynx tore. acy See Sanmeae cease 85X  85u 
EEQ@S) ejected tetas jot abechinlnataaiaragnay Mates 50X 28-30u 


Stafford (1904) names a new species Derogenes plenus briefly described 
from the wolf fish. The single specimen from that host in the present 
collection showed no specific difference from D. varicus and there appeared 
no justification for assigning it to a different species. Whether or not it 
represents Stafford’s form is, of course, unknown; but in view of the meager 
description of D. plenus the species seems somewhat uncertain. 


104 ILLINOIS BIOLOGICAL MONOGRAPHS [230 


HIRUDINELLA FUSCA* (POIRIER 1885) 
[Figs. 75-79] 


Synonyms: Dist. fuscum Poir. 
Dist. verrucosum Poir. 
Dist. clavatum of Linton 
From Stomach, Xyphias gladius (Sword fish) Woods Hole 


This trematode belongs to the interesting group of large forms repre- 
sented by Dist. clavatum. Considering the early discovery and long history 
of trematodes of this group, precise knowledge of their internal structure 
is rather meager. The history and synonymy of the group has been given 
by Poirier (1885), Buttel-Reepen (1903), and Miihlschlag (1914) and will 
not be discussed here. The group itself is well isolated (although referred 
to by Odhner as representing a sub-family of the Hemiuridae), yet the 
species within it are remarkably similar. The early custom of dependence 
on external features has led to confusion and uncertainty of species. 
Poirier’s work (1885), while dealing in detail with the morphology of the 
group, does not bring out clear distinction between species. The later 
work of Buttel-Reepen and Miihlschlag has separated with considerable 
definiteness the following species which evidently should all be referred 
to the genus Hirudinella: Dist. clavatum, Dist. ampullaceum, Dist. seimersi, 
Dist. fuscum, and Dist. ingens. The Dist. insigne of Poirier is a synonym 
of Ofodistomum veliporum, and his Dist. verrucosum is considered by Miihl- 
schlag as identical with Dist. fuscum. 

In his various papers from Woods Hole, Linton records Dist. clavatum 
from the stomach of Xyphias gladius. He describes the form to some 
extent in his 1896 paper. Cooper (1915) identifies as Hirudinella clavata 
trematodes collected from the stomach of Thunnus thynnus in Canadian 
waters. The present material from Xyphias gladius at Woods Hole is very 
probably the same form recorded by Linton. Since Linton’s description 
is incomplete and since the more recent work of Miihlschlag emphasizes 
new specific characters in the genus, a brief description of this form might 
be of some importance. 

One vial of the material contained 60 specimens varying from 7 to 
23 mm. in length and from 2.5 to 5 mm. in width. The body is very robust, 
stout, thick, and very cylindrical especially posterior to the ventral sucker. 
The posterior end is broadly rounded. The neck region is smaller than the 
swollen hindbody, and in a 23 mm. specimen measured about 6 mm. in 
length. The body is marked by transverse folds or wrinkles characteristic 
of the group and due to body contraction. The ventral sucker is very 
prominent with wide, sometimes wrinkled or corrugated margins. Its 
width is often greater than the width of the body (Figs. 76-77). Ina 


* Collection of Dr. H. B. Ward, vials Nos. 13.44 and 13.45, 


231] SOME NORTH AMERICAN FISH TREMARODES—MANTER 105 


12 mm. specimen, the oral sucker was 1.17 mm. in diameter, the ventral 
sucker 2.19 mm., and the pharynx 0.64 0.42 mm. 

The extraordinarily thick body wall is made up of (1) a thick cuticula, 
(2) a “sub-cuticular” layer in which occur (especially in the neck region) 
circular and longitudinal muscle fibers, (3) a thick circular muscle layer, 
and (4) an inner layer of longitudinal muscles. Internal to this last layer 
there occurs a well-defined cellular layer which has been called the sub- 
cuticular cellular layer. The condition of these layers were found as 
reported by Miihlschlag. The circular layer is more prominent anteriorly. 
In the mid-body regions the longitudinal layer is enormously developed 
and the fibers are grouped into conspicuous bundles. This layer may repre- 
sent the internal parenchyma muscles of Otodistomum and Azygia. 

The oral sucker opens directly into the pharynx. There is a strongly 
developed esophagus which, in contracted specimens, leads dorsally and 
anteriorly from the posterior end of the pharynx. The esophagus splits 
before losing its cuticular lining, and the lumen of each branch expands 
into a roomy tube. These two esophageal expansions open into the anterior 
regions of the intestinal ceca. Here the ceca are modified into swollen, 
bulb-like regions characterized by cells with extremely long, cilia-like 
processes which practically fill the wide lumen. These modified regions 
have been called glandular. They lead abruptly into the ceca proper which 
are lined with small cells having short, cilia-like processes. The ceca stretch 
to the posterior end of the body, and become very large in regions posterior 
to the ventral sucker, filling the greater part of the large body of the 
worm. Considerable amount of black food substance occurs within the 
intestinal ceca. 

Excretory vessels permeate all regions of the parenchyma, so that 
almost any section through the trematode shows cross-sections of numerous 
tubes of this system. There is an unpaired excretory vesicle extending as 
a laterally flattened tube between the two enormousceca. This vesicle 
opens to the exterior through a short duct provided with circular, longi- 
tudinal, and oblique muscles. The plexus of accessory excretory tubes is 
very complicated. The unpaired vesicle divides into two branches just 
behind the posterior limit of the uterus and vitellaria, or about half way 
between the posterior and anterior ends of the body. The lateral branches 
evidently wind and bend extensively, and the accompanying plexus of 
various sized vessels continue into the region of the oral sucker. 

The genital pore is median, ventral, and nearer the oral sucker (Linton 
gives its position as mid-way between the suckers). In material of the 
present studies it occurred about opposite the posterior end of the pharynx. 
It leads into a very large genital atrium which is somewhat flattened 
parallel with the ventral body surface (Fig. 75). The genital opening is 
near the anterior limit of this atrium. A conspicuous genital papilla 


106 ILLINOIS BIOLOGICAL MONOGRAPHS [232 


projects into the atrium from its dorsal surface and on the truncated tip 
of this papilla the male sex duct opens. The vagina does not enter the 
papilla. Its opening is posterior to this papilla and separated from it by 
a depression in the atrium wall. This widely separated position of the 
openings of the sex ducts into the atrium is characteristic for H. fusca and 
Figure 75 shows almost exact agreement with Miihlschlag’s diagram of 
that region. In H. clavaia, the two ducts open close together on a common 
papilla (Poirier 1885). 

The testes lie obliquely behind one another close behind the ventral 
sucker which they may slightly overlap dorsally. The somewhat coiled 
seminal vesicle leads into the duct of the large prostate gland. The prostate 
gland is lined with cells bearing cilia-like processes. The prostate gland 
coils slightly. At the base of the genital papilla the duct changes abruptly 
into the ejaculatory duct. This duct possesses a very thick inner coat of 
cuticula, and a powerful layer of circular muscles. It is, moreover, pro- 
vided with numerous muscles which attach themselves to its outer wall 
These muscles run obliquely through the papilla, and dorsal to it some of 
them are seen to lead anteriorly to the longitudinal body muscles of the 
dorsal side. Others, leading posteriorly, split off from the longitudinal 
muscles of the uterus. Still others seem to be connected with longitudinal 
body muscles of the ventral and lateral sides (Fig. 79). 

In Dist. ingens and Dist. ampullaceum where the two ducts open in 
common, special musculature surrounds not only the ejaculatory duct 
but also the terminal region of the vagina. This common muscular system 
surrounding both ducts was called a cirrus sac by Buttel-Reepen (1903), 
but that it could not be correctly interpreted as such was pointed out by 
Miihlschlag who called it the ‘‘genital musculature.” This condition of 
both sex ducts being surrounded by a common musculature brings to mind 
the so-called “cirrus sac’? about the genital sinus in some Hemiurids. 
Homologies would be difficult to draw, however, since the genital sinus in 
the latter case is probably a composite of the true genital atrium and the 
fused sex ducts. 

The ovary is located just posterior to the testes. The ootype lies in 
contact with it posteriorly and ventrally. Both organs are surrounded by 
a fibrous membrane some of the fibres of which seem to bind the two 
together as in Otodistomum. The left vitelline duct runs between the 
ootype and ovary to unite with the right duct somewhat to the right of 
the middle line. The common vitelline duct penetrates the ootype anteri- 
orly. It unites with the oviduct within the ootype. Laurer’s canal also 
penetrates the membrane of the ootype. It enters more toward the pos- 
terior, although likewise from between ovary and ootype. This canal is 
very powerfully developed with a cuticular lining and a thick wall of 
circular muscles. It is unusually long, since the ootype is near the ventral 


233) SOME NORTH AMERICAN FISH TREMATODES—MANTER 107 


surface and the canal opens to the exterior dorsally at about the level of 
the ovary. After its penetration into the ootype, it opens into a swollen, 
bulb-like enlargement which lacks the muscular coat. This swollen region 
in turn leads into a narrow duct which opens into the oviduct slightly 
before the vitelline duct (Fig. 78). The thin-walled enlargement of Laurer’s 
canal seems to. be morphologically a true seminal receptacle. No sperma- 
tozoa, however, were seen anywhere along the length of the canal. 

The uterus coils posteriorly between the intestinal ceca to a point 
about half way between anterior and posterior ends of the worm. It then 
coils anteriorly, extending dorsal to the ovary and testes, ventral to the 
seminal vesicle, and opening into the atrium as already indicated. At 
about the level of the ovary the character of its wall changes and inciudes 
circular and longitudinal muscle layers, and, outside the latter, a dense 
layer of small coils of supposedly glandular function. Overhanging, lip- 
like folds of the atrium about the opening of the vagina may serve as a 
valve to prevent re-entrance of eggs into the vagina from the atrium which 
is often well filled with them. Furthermore, out-pocketings of the vagina 
close to its tip results in forming a second valve-like fold within the vagina 
itself (Fig. 79). The constancy of this structure is, however, unknown. 

The vitellaria are tubular and winding. They occur laterally on each 
side of the body. Anteriorly they reach to about the level of the testes, 
and posteriorly as far as the posterior extent of the uterus. The rather 
thin-shelled eggs are broadly ovoid and measure about 32 by 25y. 

From the morphological features discussed above, it is evident that the 
species must be referred to H. fusca. Most characteristic is the nature of 
the genital atrium. Miihlschlag gives also the following specific characters: 
the short, thick-set body form; the swollen borders of the ventral sucker; 
and the bulb-like swelling of Laurer’s canal within the ootype. 


SIPHODERA VINALEDWARDSII* (LINTON 1899) 
[Figs. 80-83] 

From Opsanus taz (Toad fish), Woods Hole 

Synonym: Monostomum vinaledwardsti Lint. 1899 

This form was first named and imperfectly described as Monostomum 
vinaledwardsii. This original material was obtained by Linton, also from 
the toad-fish at Woods Hole. In 1911 Linton found further material of 
the same species from Ocyurus chryurus at Tortugas. He corrects and 
extends his former (1899) description and places the form in a new genus 
(Siphodera) of the distomes. This genus with a few other genera from the 
same region (Tortugas) he includes in the new family Siphoderidae. 

The present form agrees very largely with Linton’s later description. 
As he was, however, uncertain in regard to some points, the form will be 
briefly described here. 


*Collection of Dr. H. B. Ward, vials no 22.217, 22.218. 


108 ILLINOIS BIOLOGICAL MONOGRAPHS [234 


The body shape is broadly oval in outline and somewhat pointed at 
each end. It is somewhat flattened but is thicker in the middle regions, 
An average sized specimen measured 1.88 mm. in length, 1.33 mm. in 
width, and 0.53 mm. in greatest thickness, which was through the region 
of the ventral sucker. The body surface is covered with minute scale-like 
spines. The circular oral sucker is at the anterior end. In regard to the 
ventral sucker, Linton (1911) says: ‘‘The ventral sucker is a part of the 
genital apparatus (cirrus) and is depressed in a circular pit of the body wall. 
The border of the pit is muscular and has strong muscular fibers radiating 
from it.’ This description applies to the position of the ventral sucker, 
the bordered pit and radiating muscles being conspicuous even in toto- 
mounts, but the sucker itself has no direct connection with the genital 
system. The common opening of the sex ducts is just anterior to the 
sucker and just within the border of the pit (Fig. 83), as will be shown 
later. The sucker is therefore referred to in this paper as the ventral sucker 
instead of using Linton’s term ‘“‘genital sucker.”” This sucker is smaller 
than the oral sucker, and is located a little less than 1/3 the body length 
from the anterior end. In a 1.8 mm. specimen the oral sucker measured 
0.2 mm. in diameter and this ventral sucker only 0.09 mm. The diameter 
of the genital pit (which incloses both the genital pore and the ventral 
sucker) was 0.16 mm. The ventral sucker may be protruded from the pit 
(Fig. 82). There is a short pre-pharynx, globular pharynx, and short swollen 
esophagus. The intestinal ceca are widespread and reach almost but not 
quite to the posterior tip of the body. 

The excretory system is very simple. The unpaired excretory vesicle 
occupies a large part of the central region of the hind-body. It opens at the 
posterior end through a short duct which is surrounded by deeply staining 
cells. Just posterior to the ovary or not far behind the ventral sucker, the 
vesicle splits into two lateral branches which continue forward and end 
blindly beside the oral sucker. They occur internal to the intestinal ceca, 
cross them ventrally in the region of the esophagus, and run on each side 
of the pharynx. 

The musculature of the body wall is poorly developed. There is a weak 
circular layer and a longitudinal layer of somewhat separated bundles. 
The powerful diagonal muscle bands which run out obliquely and laterally 
from the border of the genital pit seem to originate in the neighborhood of 
the longitudinal body muscles. The ventral sucker is provided with two 
strong muscles which are attached to its outer border laterally and lead 
almost directly dorsally to the region of the seminal vesicle (Fig. 82). 
The body parenchyma is very loose and open. 

The testes are in two groups in the lateral regions of the middle of the 
body. The number is variable, usually 4 or 5 on each side. They are 
located near the dorsal surface, so that ventrally they are considerably 


235] SOME NORTH AMERICAN FISH TREMATODES—MANTER 109 


concealed by the egg-filled coils of the uterus. The seminal vesicle is median 
in position, anterior to the testes, with its anterior limit over-reaching the 
posterior border of the ventral sucker. It is swollen tube-like in form and 
slightly coiled. Its walls are quite thick and evidently muscular, although 
the direction of the fibers could not be made out. At about the level of 
the ventral sucker it bends ventrally and is constricted off (by an inward 
continuation of its wall) from a succeeding bulb-like portion (Fig. 83). 
This latter region leads ventrally tapering, carrot-like. Its outer wall is 
also heavy like that of the seminal vesicle. The distal portion represents 
the ejaculatory duct. A short distance before it reaches the genital pore, 
it is joined ventrally by the vagina. The common opening is very close 
in front of the ventral sucker and within the anterior border of the genital 
pit. The distal bulb-like region of the male system is evidently what 
Linton referred to as ‘‘the prostatic portion of the cirrus pouch.” Its inner 
wall is lined by what seems to be a layer of tall delicate cells, but these 
were indistinct and no nuclei could be made out. From material at hand, 
which seemed to be in good condition, it could not be definitely concluded 
that this region was glandular. As Linton studied fresh material, and as 
the cells in this region show very prominently in his figure (Linton 1911), 
his conclusion is probably correct. 

The ovary is a much lobed organ located near the ventral surface a 
short distance posterior to the ventral sucker or about at the level of the 
posterior end of the seminal vesicle. The vitellaria are composed of 
numerous small follicles located nearer the dorsal surface and extending 
laterally across the body in the region between the ventral sucker and the 
anterior testes. 

Linton’s description is somewhat incomplete in regard to the region of 
the oviduct. Laurer’s canal is present. It follows a practically straight 
course from the dorsal surface to the oviduct. Just before it enters the 
oviduct, it enters the very large, spherical seminal receptacle. This con- 
spicuous organ is located just dorsal to the ovary and between it and the 
posterior end of the seminal vesicle (Fig. 83). The common vitelline duct 
is long, and enters the oviduct shortly beyond the entrance of Laurer’s 
canal. The relations of these ducts are shown diagrammatically in Figure 
81. A few small cells about the oviduct in this region probably represent 
a poorly developed ootype. The uterus coils posteriorly on the left side of 
the body, returning on the right. When it has returned to about the level 
of the ovary, it extends across the body and proceeds anteriorly on the 
left side of the seminal vesicle to join the ejaculatory duct. There is a very 
short genital sinus. The eggs measure 22 by 10 to 12u. 

The large pyriform cells in the cortical parenchyma region of the an- 
terior part of the body were noted. Linton suggests that they represent 


110 ILLINOIS BIOLOGICAL MONOGRAPHS [236 


yolk-forming cells, but present material offered no evidence as to their 
function. 


DEROPRISTIS INFLATA* (MOLIN 1859) 
From ihtestine, Anguilla chrysypa, Woods Hole. 


This well-known parasite of the eel has already been clearly and fully 
described by Odhner (1902). The only other species in the genus is D. his- 
pida (Rud.) from the sturgeon. Stafford (1904) records D. inflata from the 
eel, but Linton does not report it from Woods Hole. 

The lateral expansions of the neck region are very characteristic for 
the genus. The body is covered with spines which are larger on the neck 
expansions and on a hump-like region on the dorsal surface opposite the 
pharynx. Odhner sees in the spined neck-expansions the fore-runner of 
the spined collar of Echinostoma. The two suckers are small and about 
equal in size. The testes are located in the extreme posterior end of the 
body, the ovary being about in the mid-body region. The vitellaria of 
small follicles extend in lateral and dorsal body regions from a point about 
half way between the ovary and ventral sucker to the anterior end of the 
anterior testis. The genital pore is median close in front of the ventral 
sucker. The genital sinus is tube-like. Both cirrus and vagina are promi- 
nent and armed with spines as in Stephanochasmus, a related genus. 

The number of neck spines could not be counted, but the species can 
be assigned to D. inflata on (1) body size, (2) relatively short genital 
sinus, and (3) egg size. The body size varied from about 0.8 mm. to 
+.mm. The genital sinus has a length about equal to the diameter of the 
ventral sucker. The egg size was 43 to 48 by 20 to 22y. 


ACANTHOCOTYLE VERRILLI GOTO 1899 
[Figs. 86-88] 
From Body surface, Raia erinacea (Bonnet skate) 


A single specimen of a trematode which seems to belong to this species 
was obtained from Raia evinacea. The parasite was found in the content 
of the spiral valve but this was, of course, an accident. It is an ectoparasitic 
form. The species was described by Goto in 1899 from a single specimen 
sent him by Verrill who obtained it from the surface of a “skate”? (from 
Cape Cod). 

In regard to general shape and form, Goto (1899:284) says: “.... the 
body is of almost uniform breadth, and presents a slightly concave border 
anteriorly. There is also a distinct constriction at the level of the pharynx. 
The posterior sucker is large and circular, and has 34 radii consisting of 


* Collection of Dr. H. B. Ward, vials no. 22.217 and 22.218. 
* Collection of Dr. H. B. Ward, vial no. 13.72. 


237) SOME NORTH AMERICAN FISH TREMATODES—MANTER 111 


numerous hollow chitinous hooks. These radii leave the central area of the 
sucker free, and the most posterior four or five pairs gradually decrease 
in length backwards, so that there is a backward extension of the central 
area. The longest radii consist of about eleven hooks and the shortest of 
only four.’’ This description of body shape, and posterior sucker fits the 
present specimen exactly, except that the posterior sucker of the latter 
has 32 radii of hooks. But Goto’s figure shows 32 instead of the 34 described 
in the text, so that this latter number is probably a misprint. In regard 
to the small accessory sucker, Goto says: ‘‘At the hind end of the posterior 
sucker there is, in the median line, a roundish appendage armed with 
filiform chitinous hooks somewhat like the upper part of an interrogation 
point. I cannot exactly state the number of these hooks, but I counted 
more than twenty.” These hooks were very clear in my specimen. There 
were 14 hooks arranged about the circumference of the sucker and two 
larger hooks in the center (Fig. 87). The body size of my specimen was 
3.3 mm. by 0.93 mm. The diameter of the posterior sucker was 1.33 mm. 
and that of the accessory sucker 0.1 mm. 

Goto claims that the anterior suckers are absent in this species and 
that “their places are occupied by two invaginations of the investing 
membrane of the body..... The invaginations are narrow and deep, 
and appear like slits in the mounted specimen” (p. 284). He claims a 
similar condition for A. lobianchoi and believes Monticelli mistaken in 
referring to the invaginations as suckers. Monticelli (1904:73-74) dis- 
agrees with this view, pointing out that suckers are actually present but 
often quite completely retracted. Monticelli, in studying many individuals 
of this genus, found most varying appearances of the suckers due to 
contraction. The complete embedding of the suckers in the body by 
contraction is a very common reaction to the killing solution. Monticelli 
interprets Goto’s figure as showing this condition. Study of my specimen 
supports Monticelli in this view. The elongate suckers with lip-like borders 
were clearly separate, especially at their margins, from the body wall 
although the internal boundaries of the suckers were indistinct. 

The mouth is median and ventral about 0.26 mm. from the anterior 
end. It leads directly into a large, somewhat triangular-shaped pharynx. 
No esophagus could be seen. The intestine branches immediately and the 
ceca extend to the posterior end of the body. 

There are about 52 testes. The exact number was difficult to determine 
as some of these organs were so close together as to seem double in nature 
Goto gives the number as only 37. The number is probably variable. 
They fill the inter-cecal space of the body in the posterior two thirds of its 
length. The seminal vesicle shows the regions characteristic of the genus. 

The ovary is spherical. It is located about 1/3 from the anterior end 
and slightly to the left. The two vitelline ducts lead to a point at its 


112 ILLINOIS BIOLOGICAL MONOGRAPHS [238 


anterior end. The vitellaria are extensive and well developed. They consist 
of large compact follicles, flattened against each other longitudinally. They 
are located laterally on each side of the body, and partially surround and 
conceal the intestinal ceca. 

Monticelli (1904) questions Goto’s observations on the sexual openings. 
Goto himself says (1899:285): ‘‘The terminal portions of the genital ducts 
could not be satisfactorily made out in the single specimen at my com- 
mand.” Goto figures a single, common genital pore on the right side of 
the body in the neck region. There are, however, normally in this genus 
three sexual openings, one lateral opening of the metraterm, while the male 
aperture is close to the opening of the vagina in a more median position 
(cf. Monticelli 1899, Tav. 1, fig. 6; Tav. 2, figs. 29-31). Monticelli (1904: 
71-72) concludes from Goto’s figure and description that actually .... 
“the mouths of the genital ducts are arranged, fundamentally, as in all 
the other species of the genus.’”’ My material shows Monticelli to be 
correct. The male aperture is very close to the opening of the vagina at 
about the level of the forking of the intestine and slightly to the right. 
What Goto interpreted as the common genital pore is actually the opening 
of the metraterm. It is located laterally on the right side of the body. 
From it protrudes in my specimen a cluster of three eggs. These eggs are 
bright yellow in color and measure 0.428 by 0.085 mm. The stalk-like 
basal region of the eggs was inserted in a swollen terminal region of the 
metraterm. 

Monticelli (1904) also expresses the conviction that Goto was wrong in 
regard to the metraterm opening to the right of the ventral face, believing 
that further study would show it to be on the left as in other species of 
Acanthocotyle. He suggests that Goto might have confused the dorsal 
with the ventral surface. In my specimen there is no doubt, however, 
that the pore is on the right side. The mouth opening could be made out 
so that the ventral surface was definitely ascertained. There remains the 
possibility that both my specimen and that of Goto represent cases of 
amphitypy, as, indeed, Monticelli suggests might occur in this group as 
found by Cerfontaine (1900:449) so common among the Octocotylides. 
Only more abundant material can settle this point. 


DACTYLOCOTYLE MINOR (OLSSON 1868) 
[Figs. 84-85] 
Synonyms: Octobothrium palmatum S. minor Olss. 1868. 
Octobothrium minus Olss. 1876. 
From Gills, Urophycis chuss (Squirrel hake) 
This species was first named by Olsson (1868:18) as a variety of 
O. palmatum Leuckart. In 1876, Olsson (1876:10) named it Octobothrium 
minus ni. sp. Cerfontaine (1898:302) observed that this species was prob- 


239] SOME NORTH AMERICAN FISH TREMATODES—MANTER 113 


ably a true Dactylocotyle species. Saint-Remy (1898:55) listed it as 
“‘Dactylocotyle minor Olss.’”’ Stiles and Hassall (1908) list the species as 
“‘Dactylocotyle minor Saint-Remy.” As Olsson’s original description of 
O. palmatum {. minor is fairly complete and accompanied by a figure, and 
since sub-specific names follow the same rules as specific names, there can 
be no reason for not retaining Olsson’s original name minor, as Saint-Remy, 
in fact, did. The correct name is then Dactylocotyle minor (Olss.) Saint- 
Remy. 

The following is a diagnosis of this species as given by Saint-Remy 
(1892:41): “Body flattened, divided into two parts by a deep indentation; 
anterior part lanceolate-oval, the posterior or caudal part much shorter 
than the anterior, provided with canals, carrying on each side 4 marginal 
pediceled suckers, pedicels cylindrical, equal. Testes in the median 
anterior part. Length 3 to6 mm., width 1.5 mm. On gills of Gadus melanos- 
tomus.”’ 

Three specimens were collected from the gills of a single fish. Examina- 
tion of numerous other fish showed no infection, so the parasite is probably 
not a very common one. In some respects the form seems to differ slightly 
from Dact. minor, but in view of the fact that body contraction partly 
explains these differences and that only three specimens were collected, 
they are referred to this species. 

Stafford records Dactvlocotyle phycidis from the gills of the squirrel hake 
in Canada. Considering the identity of region and host, it is probable that 
he was dealing with the form now being considered. The species cannot be 
referred to Dact. phycidis (although the hosts are similar) because of its 
marked difference in size, shape, and number of hooks in the genital sucker. 
It is like Dact. palmatum in possessing a common genital opening, 14-16 
hooks in the genital sucker, and in having few non-filamented eggs in the 
vagina. Olsson’s variety Dact. palmatum minor differs from Dact. palmatum 
in its smaller size and in the sharp division of its body into two regions. 

In my material, the posterior region bearing the pediceled suckers or 
pincers was so distinctly cut off from the body proper as to appear ap- 
pendicular (Fig. 84). Except for small branches from the intestine which 
invade this posterior part, all the organs are located in the anterior region. 

The anterior region is flattened and broadly oval in shape. In life it is 
of a gray color. The surface of the body is not entirely smooth, and in this 
respect my material differs from the descriptions of all other representatives 
of the genus. Minute scale-like plates give the body a roughened surface 
particularly in posterior body regions and on the pedicels of the suckers. 
These scales are less conspicuous anteriorly where the body seems quite 
smooth. 

Other features are in accord with descriptions of the genus. The pos- 
terior suckers are provided with a very complicated system of chitinous 


114 ILLINOIS BIOLOGICAL MONOGRAPHS {240 


supporting rods which make the suckers more like pincers in function. On 
each side of the mouth which is at the anterior tip of the body there is a 
small lateral sucker. A globular pharynx is present. The ceca of the 
intestine are profusely branched and the fine branches ramify throughout 
the whole body. 

The genital pore is located on the ventral surface about 0.3 mm. from 
the anterior end. Its position can be located by the conspicuous genital 
bulb or sucker. This sucker actually surrounds the distal portion of the 
male duct. It is provided with a ring of 14 hooks (Fig. 85). The number of 
hooks in the genital sucker varies within narrow limits in a species. The 
testes are numerous. Packed closely together, they fill most of the mid- 
body region of the anterior part of the worm. The seminal vesicle is located 
far forward, dorsal and slightly posterior to the genital sucker. It is much 
coiled. Between it and the genital sucker is a swollen, bulb-like region 
with very thick walls. This structure is about the size of the pharynx 
near which it is located. 

The compact and dense follicles of the vitellaria fill the sides of the body 
and almost meet just anterior to the ovary. The ovary is slightly but 
tightly coiled so that it is compact S-shaped. There is a large coiled 
seminal receptacle located slightly anterior to the ovary. An ootype and 
small yolk reservoir lie ventral to the ovary. The uterus leads a straight 
course anteriorly and joins the male duct ventrally outside the genital 
sucker and close to the genital pore. Only one non-filamented egg was found 
in the uterus. 

Measurements on two specimens are as follows: 


Teenie thin gst senckiracey o wane oat Seteions 2.8 mm. 2.9 mm. 

Widthtegeckctien ciicuneuearornunentrate ora ans 1.6 mm. 1.75 mm. 

Oral sucker cob yeeros esac. ... 0.108 0.114 

Genital suckerawiac ae. aais. ascites 2 ot ean 0.074 0.085 

Beara cise eect eee sin: 0.159 by 0.017 

Longest diameter of posterior suckers—1. .0.188 0.199 
2..0.245 0.21 
3..0.381 0.228 


4.. 0.399 


_ 241] SOME NORTH AMERICAN FISH TREMATODES—MANTER 115 


SUMMARY AND CONCLUSIONS 


A general collection of entozoa of marine fish was made at Mt. Desert 
Island, Maine. Of these parasites, the trematodes were selected for study. 

Particular attention was given to Otodistomum cestoides from the 
stomach of Raia stabuliforis. The morphology of this form was studied in 
considerable detail and compared with O. veliporum, material of which 
from Raia binoculata was available. The two species were found to be 
even more similar than hitherto recorded, but were distinct in a marked 
difference in egg size. The extent of the vitellaria varied considerably and 
this feature cannot be used to separate species in this genus. The internal 
longitudinal parenchyma muscles were found to be somewhat scattered in 
these forms, but definitely external to the vitellaria, a condition to be 
contrasted with their position in the related genus, Azygia. The prominent 
genital papilla hitherto considered as a permanent structure in Otodisto- 
mum was found to have the capacity (in both species) of being completely 
flattened out, or completely protruded. It was found to be usually much 
less prominent in O. veliporum. 

The growth changes of O. cestoides within its final host were studied 
from measurements on over 200 specimens. Conspicuous changes in size 
are associated with regional changes in body proportions. Growth results 
chiefly in body elongation and occurs chiefly posterior to the ventral sucker. 
The region of the uterus slightly increases its size ratio to other body parts 
after sexual maturity, but the tail region alone also maintains a constant 
proportional growth increase as compared with the region anterior to the 
ventral sucker. The two suckers maintain a constant proportional size in 
respect to each other. Both suckers are relatively much larger in young 
forms. 

Live miracidia of O. cestoides were readily obtained by the hatching of 
eggs secured from adult worms. These eggs at the time of deposit contain 
mature larvae ready to hatch. The egg shell is, however, very thick. It was 
discovered that the hatching of the eggs was stimulated by evaporation of 
the sea-water in which they were kept. Eggs in cultures submerged in 
aquaria did not hatch. Larvae were obtained as early as five hours after 
removal of eggs from the worm. All indications point to the conclusion 
that the eggs do not normally hatch until eaten by the intermediate host. 

The miracidium of O. cestoides was found to be unciliated. Its form 
and shape vary with the worm-like extension and contraction of the body. 
The anterior end of the larva is continually being retracted and extended 


116 ILLINOIS BIOLOGICAL MONOGRAPHS (242 


like a proboscis. The miracidium has no apparent capacity for locomotion. 
A conspicuous internal organ of the miracidium has been commonly 
interpreted as an intestine. It was found that this organ was four-partite 
in structure. Each part evidently consisted of one cell with a large nucleus. 
The organ therefore cannot be regarded as an intestine, but probably 
represents a group of unicellular glands. 

The eggs of O. cestoides are eaten by snails kept in the same vial with 
them. This eating of the eggs was conspicuous only in the case of the 
common gasteropod, Littorina littorea. Larvae were found hatching in the 
intestine of this snail in two cases. 

The entire family Azygiidae was studied in an attempt to clear up an 
evident confusion in that group especially in American forms. The type 
material of most American species of Azygia and related genera was 
studied. It was found that all American representatives (consisting of 
eleven recorded forms) could all be referred to three species of Azygia as 
follows: Mimodisiomum angusticaudum Staff. and Azygia loossti Marshall 
and Gilbert to Azygia angusticauda (Stafi.); Dist. longum Leidy, Dist. 
tereticolle of Leidy, Megadistomum longum (Leidy), Azygia tereticolle of 
Stafford, Azygia sebago Ward, Azygia bulbosa Goldberger, Hassallius 
hassalli Goldberger, and Azygia lucii of Cooper to Azygia longa (Leidy). 
Azygia acuminata Goldberger was retained. Apparent differences between 
many of the forms were found to be in accord with growth changes which 
would be expected in the group. Azygia perryii was also studied and found 
to be probably identical with the European species, Azygia lucit. 

A general study was made of the entire trematode collection from 
Mount Desert Island. A few forms from Woods Hole are also considered. 
Twenty different species belonging to eighteen different genera are identi- 
fied. A number of these are described at some length. 


243] SOME NORTH AMERICAN FISH TREMATODES—MANTER 117 


BIBLIOGRAPHY 
ARIOLA, V. 
1899. Di alcuni Trematodi di pesci marini. Atti Soc. Lig. nat. e Geo., 10:3-12, Tay. 5. 
Bartow, C. H. 
1923. Life Cycle of Fasciolopsis buski (Human) in China. China Med. Jour., 37:1-20, 
7 text figs. 
BENEDEN, P. J. VAN 
1858. Memoire sur les vers intestinaux. Paris. 376 pp., 28 pls. 
1871. Les poissons des cétes de Belgique, leurs parasites et leurs commensaux. Mem. 
Acad. Roy. de Belg., 38: 100 pp., 6 pls. 
BIcELow, H. B., and WEtsu, W. W. 
1925. Fishes of the Gulf of Maine. Bull. U.S. Bur. Fish., 30:1-567, 278 figs. 
Braun, M. 
1894. Vermes-Trematodes. Bronn’s Klassen und Ordnung des Thierreichs. 4, Abt. 1: 
925 pp., 34 pls. 
ButTTEL-REEPEN, H. von 
1903. Zur Kenntniss der Gruppe des Distomum clavatum, insbesondere des Dist. ampul- 
laceum und des Dist. siemersi. Zool. Jahrb. Syst., 17:163—236, 8 text figs., Taf. 6-10. 
CERFONTAINE, P. 
1896. Contributions 4 l’étude des Octocotylides. II. Le genre Dactylocotyle. Arch. Biol., 
14:510-535, pls. 23-24. 
1898. Contributions 4 l’étude des Octocotylides. IV. Nouvelles observations sur le genre 
Dactylocotyle et description du Dactylocotyle lusceae. Arch. Biol., 15:301-328, 
3 text figs., pl. 12. 
1900. Contribution 4 ]’étude des Octocotylides. V. Les Onchocotylinae. Arch. Biol., 
16:345-476, pls. 18-21. 
Cooper, A.R. 
1915. Trematodes from Marine and Freshwater Fishes, including one species of Ecto- 
parasitic Turbellarian. Trans. Roy. Soc. Canad., Sec. IV, 9:181-205, 3 pls. 
Cort, W. W. 
1921. The Development of theJapanese Blood Fluke, Schistosoma japonicum Katsurada, 
in its Final Host. Amer. Jour. Hyg., 1:1-38, 3 text figs., 4 pls. 
CREUTZBURG, N. 
1890. Untersuchungen iiber den Bau und die Entwicklung von Distomum ovocaudatum 
Vulpian. Inaug.-Dissert., Leipzig. 32 pp. 
Darr, A. 
1902. Uber zwei Fasciolidengattungen. Zeit. wiss. Zool., 71:644-701, 1 text fig. 
Duyjarviy, M.F. 
1845. Histoire naturelle des helminthes. Paris. 654 pp. 
Fujita, T. 
1918. Onanewspecies of Azygia. Jour. Zool., Tokyo, 30:269-274, pl. 1. 
GOLDBERGER, Jos. 
1911. Some Known and Three New Endoparasitic Trematodes from American Fresh 
Water Fish. Bull. Hyg. Lab., 71:7-35, 5 pls. 
Goto, S. 
1899. Notes on Some Exotic Species of Ectoparasitic Trematodes. Jour. Sci. Coll. Imp. 
Univ., Tokyo, 12:263-295, pls. 20-21. 


118 ILLINOIS BIOLOGICAL MONOGRAPHS [244 


JAcosy, S. 
1899. Beitrige zur Kenntnis einiger Distomen. Inaug.-Dissert., Konisberg. 30 pp., 2 pls. 
JounstToN, S. J. 
1902. Contributions to a Knowledge of Australian Entozoa. No. II. Proc. Linn. Soc. 
N.S. Wales, 27 :326-330, pl. 13. 
JAGERSKIOLD, L. A. 
1900. Ein neuer Typus von Copulationsorgen bei Dist. megastomum. Central. Bakt. 
Par., 27:68-74, 4 text figs. 
Juet, H.O. 
1889. Beitrige zur Anatomie der Trematodengattung Apoblema (Dujard.). Beih. k. 
Svenska Vet.-Akad. Handl., 15:3~46, Taf. 1. 
KENDALL, Wm. C. 
1908. Fauna of New England: List of Pisces. Boston Soc. Nat. Hist., Occas. Papers, 
7:152 pp. 
LANDER, C. H. 
1904. The Anatomy of Hemiurus crenatus (Rud.) Liihe, an Appendiculate Trematode. 
Bull. Mus. Comp. Zool. Harv. College, 45:1-28, 4 pls. 
Lesoour, M.V. 
1908. Fish Trematodes of the Northumberland Coast. Rept. Northumberland Sea Fish., 
1907, 3:3-47, 5 pls. 
Lerwy, Jos. 
1851. Contributions to Helminthology. Proc. Acad. Nat. Sci. Phila., 5:205-210. 
LEIPER, R. T. AND ATKINSON, E. L. 
1915. Parasitic Worms, British Antarctic (“Terra Nova”) Expedition, Zoology. 2:19-60, 
11 text figs., 5 pls. 
Leuckart, R. 
1886. Die Parasiten des Menschen. 2te Aufl. Leipzig. 897 pp. 
LevinsEn,G. M.R. 
1881. Bidrag til Kundskab om Grgnlands Trematodfauna. Overs. Danske. Vidensk. 
Selsk. Forhdl., 1:49-84, tab. 2-3. 
Liystow, O. von 
1890. Ueber den Bau und die Entwicklung des Distomum cylindraceum Zed., Arch. 
mikr. Anat., 36:173-191, Taf. 7-8. 
1907. Zwei neue Distomum aus Luciperca sandra der Wolga. Ann. Mus. Zool. Acad. 
Imp. Sci. St. Petersbourg, 12:201—202, 1 text fig. 
LinTON, E. 
1889. Notes on Entozoa of Marine Fishes of New England. Ann. Rept. Comm. Fish 
and Fisheries for 1886:453-498, 6 pls. 
1898. Notes on Trematode Parasites of Fishes. Proc. U. S. Nat. Mus., 20:507-548, 
pls. 40-54. 
1900. Fish Parasites Collected at Woods Hole in 1898. Bull. U. S. Fish Comm. for 1899, 
19:267-304, pls. 33-43. 
1901. Parasites of Fishes of the Woods Hole Region. Bull. U. S. Fish Comm. for 1899, 
19:405-492, 34 pls. 
1905. Parasites of Fishes of Beaufort, North Carolina. Bull. U. S. Bur. Fish., 24:321- 
428, 34 pls. 
1911. Helminth Fauna of the Dry Tortugas. II. Trematodes. Carnegie Inst. Wash., 
Pub., 133:15-98, 28 pls. 
Looss, A. 
1894. Die Distomen unserer Fische und Frésche. Bibliotheca Zool., 16: 296 pp., Taf. 1-9. 
1896. Recherches sur les faune parasitaire de l’Egypte, I. Mem. I’Inst. Egypt., 3: 252 pp., 
16 pls. 


245) SOME NORTH AMERICAN FISH TREMATODES—MANTER 119 


1899. Weitere Beitrige zur Kenntniss der Trematoden-Fauna Aegyptens. Zool. Jahrb., 
Syst., 12:521-784, Taf. 24-32. 

1901. Zur Sammel und Conservierungstechnik von Helminthen. Zool. Anz., 24:302-304, 
309, 318. 

1907. Beitrige zur Systematic der Distomen. Zool. Jahrb., Syst., 26:63-180, Taf. 7-15. 

1907a. Zur Kenntnis der Distomenfamilie Hemiuridae. Zool. Anz., 31:585-620. 

Ltue, M. 

1900. Uber die Gattung Podocotyle (Duj.) Stoss. Zool. Anz., 23:487-492. 

1901. Uber Hemiuriden. Zool. Anz., 24:394-488. 

1909. Parasitische Plattwiirmer, I. Trematodes. Siisswasserfauna Deutschlands, Heft 17. 

Manter, H. W. 
1925. Some Marine Fish Trematodes of Maine. Jour. Parasit., 12:11-18, pl. 2. 
MarsHALL, W.S. AND GILBERT, N.C. 

1905. Three New Trematodes Found Principally in Black Bass. Zool. Jahrb., Syst., 

22 :477-488, pl. 15. 
MONTICELLI, F.S. 

1899, Il Genere “Acanthocotyle.” Arch. Parasit., 2:75-120, Tav. 1-3. 

1904. Osservazioni intorno ad alcune specie di Heterocotylea. Boll. Soc. nat. Napoli, 
18 65-80, 5 text figs. 

Miatscutac, G. 

1914, Beitrige zur Kenntnis der Anatomie von Otodistomum veliporum (Creplin), 
Distomum fuscum Poirier, and Distomum ingens Moniez. Zool. Jahrb., Syst., 
37:199-252 16 text figs., Taf. 9-10. 

Nico, Wu. 

1907. A Contribution towards a Knowledge of the Entozoa of British Marine Fishes. 
Part I. Ann. Mag. Nat. Hist., ser. 7, 19:66-4, 4 pls. 

1909. Studies on the Structure and Classification of the Digenetic Trematodes. Quar. 
Jour. Micr. Sci., 53:391-487, pls. 9-10. 

1909a. A Contribution towards a Knowledge of the Entozoa of British Marine Fishes. 
Part II. Ann. Mag. Nat. Hist., ser. 8, 4: 25 pp., 1 pl. 

1910. On the Entozoa of Fishes from the Firth of Clyde. Parasit., 3:322-359, pl. 29. 

1913. New Trematode Parasites from Fishes of the English Channel. Parasit., 5:238-246, 
pl. 11. 

1913a. Trematode Parasites from Food-Fishes of the North Sea. Parasit., 6:188-194, pl. 13. 

1914. The Trematode Parasites of Fishes from the English Channel. Jour. Mar. Biol. 
Assn., 10:466-505. 

1915. A list of the Trematode Parasites of British Marine Fishes. Parasit., 7:338-378. 

1915a. The Trematode Parasites of North Queensland. III. Parasites of Fishes. Parasit., 
8:22-41, pls. 4-5. 

NORDMANN, A. VON 

1832. Mikrographische Beitriige zur Naturgeschichte der wirbellosen Thiere. Erstes 

Heft. Berlin. 118pp., 10pls. 


ODHNER, T. 
1901. Revision einiger Arten der Allocreadium Lss. Zool. Jahrb., Syst., 14:483-520, 
Taf. 33. 
1902. Mitteilungen zur Kenntnis der Distomen, II. Central. Bakt. Par., 31:152-162, 
3 text figs. 
1905. Trematoden des arktischen Gebietes. Fauna Arctica, 4:291-372, 4 text figs., 
Taf. 2-4. 


1911. Zum natiirlichen System der digenen Trematoden. II. Zool. Anz., 37:237-253, 
2 text figs. 


120 ILLINOIS BIOLOGICAL MONOGRAPHS [246 


1911a. Zum natiirlichen System der digenen Trematoden. III. Zool. Anz., 38:97-117, 
8 text figs. 
1911b. Zum natiirlichen System der digenen Trematoden. IV. Zool. Anz., 38:513-531, 
2 text figs. 
1914. Cercaria setifera von Monticelli- die Larvenform von Lepocreadium album Stoss. 
Zool. Bidr. Uppsala, 3:247-255, Taf. 6. 
Otsson, P. 
1868. Entozoa, iakttagna hos Skandinaviska hafsiskar. Lund’s Univ. Arsskrift, 4:1-64, 
Tab. 3-5. 
1876. Bidrag till Skandinaviens Helminthfauna. Kongl. Svenska Vet.-Akad. Handl., 
14:3-35, Taf. 1-4. 
PEARSE, A. S. 
1924. The Parasites of Lake Fishes. Trans. Wis. Acad. Sci., 21:161-194. 
PorRIER, J. 
1885. Contribution 4 l’histoire des trématodes. Arch. Zool. experm., ser. 2, 3:465-624, 
pls. 23-34. 
Pratt, H.S. 
1898. A Contribution to the Life-history and Anatomy of the Appendiculate Distomes. 
Zool. Jahr., Anat. u. Ont., 11:3-40, pls. 25-27. 
Satnt-Remy, G. 
1892. Synopsis des trématodes monogénéses. Rev. biol. nord. France, 4: 92 pp., pl. 10. 
1898. Complément du synopsis des trématodes monogénéses. Arch. Parasit., 1:521—-571. 
SCHAUINSLAND, H. 
1883. Beitrige zur Kenntnis der embryonalen Entwicklung der Trematoden. Jen. Zeit. 
Naturwiss., 16:465-527, Taf. 19-21. 
Scott, T. 
1909. Some Notes on Fish Parasites. 26th Ann. Rept. Fish. Bd. Scot., 3:73-92, pls. 3-7. 
SIEBOLD, C. TH. von 
1837. Zur Entwickelungsgeschichte der Helminthen. K. F. Burdach’s: Die Physiologie 
als Erfabrungswissenschaft. Bd. 2, 2 Aufl. Leipzig. 
STAFFORD, J. 
1904. Trematodes from Canadian Fishes. Zool. Anz., 27:481-495. 
Stires, C. H. AnD HAssatt, A. 
1898. An Inventory of the Genera and Subgenera of the Trematode Family Fasciolidae. 
Arch. Parasit., 1:81-99. 
1908. Index-Catalogue of Medical and Veterinary Zoology. Subjects: Trematedes and 
Trematode Diseases. Bull. Hyg. Lab., 37: 401 pp. 
SrossicH, M. 
1886. I distomi dei pesci marini e d’acqua dolce. Prog. Ginnasio comm. sup. Trieste, 
3-66. 
1890. Brani di elmintologia tergestina, VII. Boll. Soc. adr. sci. nat. Trieste, 11:23-30, 
pls. 13-14. 
1892. I distomi dei mammiferi. Prog. d. civ. scuola r. sup., Trieste, 42 pp. 
1898. Saggio di una fauna elmintologica di Trieste e provincie contermini. Prog. d. civ. 
scuola r. sup., Trieste, 162 pp. 
1600. Osservazioni elmintologiche. Boll. Soc. adr. sci. nat., Trieste, 20:89-103, Tav. 6. 
1903. Note distomologiche. Boll. Soc. adr. sci. nat., Trieste, 21:193-201. 
Tuomas, A. P. 
1883. The Life History of the Liver Fluke. Quart. Jour. Micros. Sci., 23:99-133. 
VAN CLEAVE, H. J. 
1920. Notes on the Life Cycle of Two Species of Acanthocephala from Fresh Water Fishes. 
Jour. Parasit., 6:167-172, pl. 14. 


247] SOME NORTH AMERICAN FISH TREMATODES—MANTER 121 


ViLtoT, M.A. 
1879. Organization et développement de quelques espéces de trématodes endoparasites 
marins. Ann. sci. nat., ser. 6, 8: 40 pp., pls. 5—10. 
WacENER, G.R. 
1857. Beitrige zur Entwicklungs-Geschichte der Eingeweidewiirmer. Naturk. Verhandl. 
Holland. Maatsch. Wetensch. Haarlem, 2 Verzamel., 13: 112 pp., pls. 1-36a. 
Warp, H.B. 
1910. Internal Parasites of the Sebago Salmon. Bull. U. S. Bur. Fish., 28:1153-1194, 
pl. 121. 
1917. On the Structure and Classification of North American Parasitic Worms. Jour. 
Parasit., 4:1-11. 
Warp, H. B. AND WHIPPLE, G. C. 
1918. Fresh Water Biology. New York. 1111 pp., 1547 figs. 
WILLEMOES-SuuM, R. VON 
1871. Uber einige Trematoden und Nemathelminthen. Zeit. wiss. Zool., 21:175-203 
Taf. 11-13. 


122 


ILLINOIS BIOLOGICAL MONOGRAPHS 


EXPLANATION OF PLATES 


[248 


With the exception of Figs. 3, 76, 77, and 81, all figures were drawn with the aid of a 
camera lucida. The scale projected is equal to 0.1 mm. unless otherwise indicated in the 
explanation of figures. The following abbreviations are used: 


tail appendage 
accessory sucker 
anterior sucker 
cuticula 

common sex duct 
circular muscles 
cirrus sac 
diagonal muscles 
duct of prostate gland 
excretory system 
equatorial fibers 
ejaculatory duct 
esophagus 
genital fold 
female sex opening 
genital atrium 
gland cell 

genital pore 
genital sinus 
intestine 
Laurer’s canal 


lm 


nef 


mo 


longitudinal muscles 
meridional fibers 
male sex opening 
ovary 

oviduct 

ootype 

ovum 

genital papilla 
pharynx 
prepharynx 
prostate gland 
radial fibers 
spermatozoa 
seminal receptacle 
seminal vesicle 
testis 

uterus 

vagina 

ventral sucker 
vitellaria 

yolk duct 


249] SOME NORTH AMERICAN FISH TREMATODES—MANTER 123 


PLATE I 


124 


Fig. 
Fig. 
Fig. 


Fig. 
Fig. 


Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 


go 


oO: 


ILLINOIS BIOLOGICAL MONOGRAPHS [250 


EXPLANATION OF PLATE I 


Otodistomum cestoides. Ventral view of adult. Scale=1 mm. 

O. cestoides. Ventral view of young specimen. 

Copy of Nicoll’s figure of cercaria of O. cestoides from cyst from flounder. Enlarged 
to same proportion as Figure 2. 

O. cestoides. Ventral view of young specimen. Scale=1mm. 

Sagittal section through anterior region of O. cestoides showing normal condition of 
genital papilla. Scale=1mm. 

Same, with genital papilla protruded. Scale=1 mm. 

Sagittal section through genital atrium of O. veliporum. 

Same of O. cestoides. 

Sagittal section through a position of ventral sucker of O. cestoides. 


10. Frontal section through pharynx region of O. cestoides. Scale=1 mm. 
11. Cross-section through edge of ovary of O. veliporum showing beginning of oviduct. 
12. Sagittal section through portion of body wall of O. cestoides. Scale=0.5 mm. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MANTER FISH TREMATODES BEATE I 


‘THE LIDRARY 
OF ie See 
eqs € HLINGLO 


teed 


251] SOME NORTH AMERICAN FISH TREMATODES—MANTER 125 


PLATE II 


126 


ILLINOIS BIOLOGICAL MONOGRAPHS [252 


EXPLANATION OF PLATE II 


Figs. 13-18. Outline drawings of gonads in O. cestoides to show changes in relative position 


Figs. 19-20. 
Figs. 21-22. 
Fig. 


23. 
BLE 
nods 
. 26. 
GAL 


aos 


neue 
- 30. 


of ovary. 

Cross-sections of Azygia sebago to show inner parenchyma muscles. 

Same of A. acuminata. 

Same of Olodistomum cestoides. 

Ootype region of O. cestoides to show relations of ducts. Semi-diagrammatic. 
Cross-section through vas deferens of O. cestoides. Scale=0.05 mm. 

Sections through early eggs of O. cestoides before shell has assumed regular form. 
Frontal section through uterus region of Azygia angusticauda, showing inner 
parenchyma muscles. 

Sagittal section through genital atrium region of O. cestoides showing genital 
papilla retracted. 

Same of O. veliporum showing genital papilla protruded. 

Ventral view of anterior body region of Asygia longa showing position of genital 
pore. Scale=1 mm. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


SioRee 
C) 


MANTER FISH TREMATODES PLATE II 


- are - 
ar 
CuIVE aaiTY GF = iuinars: 


253] SOME NORTH AMERICAN FISH TREMATODES—MANTER 4127 


PLATE III 


128 


Fig. 31. 
Fig. 32. 
Fig. 33. 


Fig. 34. 
Fig. 35. 


Fig. 36. 
Vig. 37. 
Fig. 38. 
Fig. 39. 


Figs. 40-41. 
Figs. 42-43. 
Tig. 44. 


Fig. 45. 
Fig. 46. 
Fig. 47. 
Fig. 48, 


ILLINOIS BIOLOGICAL MONOGRAPHS. ; (254 


EXPLANATION OF PLATE III 


Mature egg of Otodistomum cestoides. Drawn from live egg. Scale=0.05 mm. 
Same, showing three lobes in internal organ. Scale=0.05 mm. 

Miracidium and empty egg shell of O. cestoides. Drawn from toto-mount. 
Length of larva 914. 

Recently dead miracidium of O. cestoides showing bristle plates detached. 
Scale=0.05 mm. 

Cross-section through mature egg of O. veliporum showing the five bristle plates. 
Diameter of egg 50x. 

Longitudinal section through mature egg of O. cestoides, showing paired glands. 
Cross-section of same. 

Longitudinal section through mature egg of O. veliporum. 

Recently hatched miracidium of O. cestoides. Drawn from live specimen. 
Scale=0.05 mm. 

Cross-sections through mature eggs of O. veliporum. Diameter of eggs about 60x. 
Recently dead miracidia of O. cestoides, showing bristle plates. Scale=0.05 mm. 
Longitudinal section of mature egg of Azygia acuminata showing four nuclei 
in internal organ. Length of egg 60x. 

Lepidapedon rachion. Ventral view. 

Sagittal section through region of ventral sucker of L. rachion. 

Same of L. elongatum. 

Lepidapedon clongatum. Ventral view. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MANTER FISH TREMATODES PLATE III 


THE LIBRARY 
OF TH 


CMERTy por Pou Risa 
pala eee NS ae 


1 
Part a hed 


255} SOME NORTH AMERICAN FISH TREMATODES—MANTER 129 


PLATE TV 


130 


ILLINOIS BIOLOGICAL MONOGRAPHS {256 


EXPLANATION OF PLATE IV 


. Podocotyle atomon. Ventral view. 

. Podocotyle olssoni. Ventral view. 

. Stephanochasmus baccatus. Ventral view. 

. Sections through eggs of S. baccatus. 

. Brachyphallus crenatus. Ventral view. 

. Homalometron pallidum. Ventral view of young specimen. 

. A. pallidum. Sagittal section through region of seminal vesicle. 
. H. pallidum. Ventral view of adult. 

. Derogenes varicus. Ventral view. 

. Steganoderma formosum. Ventral view. 

. S. formosum. Cross-section through body just posterior to ovary. 
. S. formosum. Sagittal section through posterior body region. 

. Lecithaster gibbosus. Ventral view. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MANTER FISH TREMATODES PLATE IV 


THE Uhany 
OF THE 
CUMRSqy 


' Waa: 
wiede 1g 


— 


257] SOME NORTH AMERICAN FISH TREMATODES—MANTER 131 


PLATE V 


132 ILLINOIS BIOLOGICAL MONOGRAPHS [258 


EXPLANATION OF PLATE V 


Fig. 62. Ventral view of Hemiurus levinseni with tail appendage extended. 
Fig. 63. Same, with tail appendage retracted. 

Fig. 64. Ventral view of anterior body region of Genolinca laticauda. 

Fig. 65. Ventral view of entire body of G. laticauda. 

Fig. 66. Same view of another specimen. 

Fig. 67. Ventral view of Gonocerca phycidis. 

Fig. 68. Ventral view of anterior body region of same. 

Fig. 69. Sagittal section through posterior body region of G. phycidis. 

Fig. 70. Lateral view of anterior body region of A ponurus sphaerolecithus. 
Fig. 71. Ventral view of entire body of A. sphaerolecithus. 

Fig. 72. Cross-section through body of A. sphaerolecithus just posterior to sinus sac. 
Fig. 73. Ventro-lateral view of body of A. sphaerolecithus in region of gonads. 
Fig. 74. Ventral view of same. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


MANTER FISH TREMATODES PLATE V 


259} SOME NORTH AMERICAN FISH TREMATODES—MANTER 133 


PLATE VI 


134 


Fig. 
Fig. 
Fig. 
Fig. 
Fig. 


Fig. 
Fig. 


Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 
Fig. 


ILLINOIS BIOLOGICAL MONOGRAPHS [260 


EXPLANATION OF PLATE VI 


. Sagittal section through anterior body region of Hirudinella fusca. Scale=1 mm, 
. Free-hand drawing of H. fusca, lateral view. 

. Same, ventral view. 

. Composite drawing from three sagittal sections through ootype region of H. fusca. 


Sagittal section through anterior body region of H. fusca, showing detail. Scale= 
0.5 mm. 


. Ventral view of Stphodera vinaledwardsti. The eggs are omitted. 
. Diagrammatic representation of relationship of female ducts with the oviduct in 


S. vinaledwardsit. 


. Cross-section through region of ventral sucker of S. vinaledwardsii. 

. Sagittal section through same region. 

. Outline drawing of Dactycotyle minor, showing body regions. Scale=1 mm. 
. Genital sucker of D. minor. Scale=0.05 mm. 

. Posterior sucker of Acanthocotyle verrilli. 

. Accessory posterior sucker of A. verriilé. Scale=0.05 mm. 

. Ventral view of A verrilli. Scale=1 mm. 


ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME X 


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MANTER FISH TREMATODES PLATE VI 


THE LIBRARY 


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261] SOME NORTH AMERICAN FISH T REMATODES—MANTER 


INDEX TO SCIENTIFIC NAMES 


Acanthias vulgaris, 2 
Acathobothrium coronalum, 10 
Acanthocotyle, 79 
Acanthocotylinae, 79 
Acanthocotyle lobianchoi, 111 
verilli, 80, 110 
Accacoeliinae, 79, 91 
Accacoelium, 90 
Accacoelium contortum, 102 
aculeatus, Gasterosteus, 94 
acuminata, Azygia, 57, 61, 72, 78, 116 
adspersus, Tautogolabrus, & 
Aega psora, 9 
aeglifinus, Melanogrammus, 9, 84 
afinis, Brachyphallus, 94 
album, Lepocreadium, 86 
Allocreadiidae, 79 
Allocreadiinae, 79 
Allocreadium atomon, 81 
Alosa finta, 92 
americanus, Pseudopleuronectes, 3 
Amica calva, 61 
Ammiatus caluus, 61, 72 
Ammodytes tobianus, 94 
ampullaceum, Distomum, 104 
Anarrhichas lupus, 9, 81, 103 
Anguilla chrysypa, 9, 72, 94, 110 
anguillaris, Zoarces, 9 
anguinea, Chlamydoselache, 14 
angulatum, Distomum, 80 
angusticauda, Azygia, 60, 78, 116 
angusticaudum, Mimodistomum, 60, 116 
Apoblema mollissimum, 91, 95 
Aponurus, 79 
Abonurus laguncula, 98 
Aponurus sphaerolecithus, 80, 98 
appendiculatum, Distomum, 93 
appendiculatus, Hemiurus, 93 
atomon, Allocreadium, 81 
Distomum, 80 
Podocotyle, 79, 81 
Azygia, 18, 54 
Azygia acuminata, 57, 61, 72, 78, 116 
angusticauda, 60, 78, 116 
bulbosa, 61, 68, 116 
longa, 63, 72, 78, 116 
loossii, 60, 74, 116 
lucii, 45, 51, 63, 68, 73, 116 
perryii, 69, 74 
robusta, 64, 73, 77 
sebago, 30, 63, 67, 77, 116 
tereticolle, 58, 63, 69, 116 
volgensis, 77 
Azygiidae, 49, 54, 79 


baccatus, Stephanochasmus, 79, 83 
Bathycotyle, 102 

batis, Raia, 14, 43 

binoculata, Raia, 14, 41, 115 
bothryophorus, Hemiurus, 95 
botryophoron, Lecithophyllum, 98 
botryophoron, Distomum, 95 
Brachyphallus, 79, 90 
Brachyphallus affinis, 94 
Brachyphallus crenatus, 80, 94 
Buccinum undatum, 52 

buski, Fassciolopsis, 29 

bulbosa, Azygia, 61, 68, 116 


callarias, Gadus, 9, 82, 92, 103 
calva, Amia, 61 

calvus, Amiatus, 61, 72 

capito, Mugil, 92 

conicula, Scyllium, 43 
Carcharias milberti, 43 
Carcharias rondeletti, 43 
Carcharias sp., 43 
Centrolophus pompilus, 43 
cestoides, Distomum, 14, 52 


Otodistomum, 10, 14, 29, 41, 44, 50, 75, 115 


Charopinus dalmanni, 10 

Chimaera monsti‘osa, 43 
Chlamydoselache anguinea, 14 

chrysypa, Anguilla, 8, 10, 72, 94, 110 

chuss, Urophycis, 9, 92 

chyurus, Ocyurus, 107 

cinereus, Notidanus, 43 

clavata, Hirudinella, 55, 59, 91, 104 

clavata, Raia, 14, 43 

clavatum, Distomum, 54, 104 

Clupea harengus, 8, 94 

communis, Hemiurus, 93 

confusus, Lecithaster, 96 

contortum, Accacoelium, 102 

coronatum, Acanthobothrium, 10 

Cottus, scorpius, 93 

crenatus, Brachyphallus, 80, 94 

cylindracea, Haplometra, 49 

cylindraceum, Distomum, 29, 47 

cylindratus, Neoechinorhynchus, 10 

cynoglossus, Pleuronectes, 53 


Dactylocotyle, 79 
Dactylocotvle minor, 80, 112 

palmatum, 113 

phycidis, 113 
dalmanni, Charopinus, 10 
Derogenes, 77, 88, 98, 102 
Derogenes varicus, 78, 103 
Derogenes plenus, 103 
Deropristis, 79 


136 ILLINOIS BIOLOGICAL MONOGRAPHS {262 


Deropristis inflata, 80, 110 
hispida, 110 

diaphanes, Raia, 8 

Digenea, 79 

Dinurinae, 91 

Dinurus, 79 

Diphterostomum, 88 

Distomata, 79 

Distomum ampullaceum, 104 

Distomum angulatum, 80 
atomon, 80 
appendtculatum, 93 

Distomum botryophoron, 95 

Distomum botryophoron, 95 
cestoides, 14, 52 
clavatum, 54, 104 
cylindraceum, 29, 47 
Suscum, 104 
hispidum, 29 
ingens, 104 
insigne, 43, 59, 104 
lanceolatum, 45 
longum, 63, 66, 72, 116 
megastomum, 55 
microcephalum, 42 
mollissimum, 95 
ovocaudatum, 46 
rachion, 84 
rosaceum, 45 
scymnt, 43 
siemerst, 104 
simplex, 80, 83 
tereticolle, 50, 58, 63, 69, 116 
variegalum, 49 
veliporum, 14, 43, 55 
verrucosum, 55, 107 
volgense, 77 

dolomieu, Micropterus, 72 


Echinorhinus spinosus, 43 
elongata, Lepodora, 85 
elongatum, Lepidapedon, 80, 85 
eperlanus, Osmerus, 94 
erinacea, Raia, 8, 110 
erinaceus, Rhynchobothrius, 10 
Esox estor, 65 
lucius, 65, 72 
masquinongy, 65, 72 
reticulatus, 66 
estor, Esox, 65 
euxinus, Gadus, 92 


Fasciola squali griset, 43 
hepatica, 29, 34 
ventricosa, 55 

Fasciolopsis buski, 29 

Fellodistominae, 88 

Serruginea, Limanda, 9 

finta, Alosa, 92 

flavescens, Perca, 72 

Sormosum, Steganoderma, 79, 88 

fullonica, Raia, 14, 43 

Fundulus heteroclitus, 9, 86 

Susca, Hirudinella, 59, 80, 104 

fuscum, Distomum, 104 


Gadus callarias, 9, 82, 92, 103 
euxinis, 92 
melanostomits, 113 
morrhua, 93 

garrardi, Lepidapedon, 84 

garrardi, Lepodora, 84 

Gasterosteus aculeatus, 94 

Genarches, 91, 100 

Genolinea, 79, 100 

Genolinea laticauda, 80, 100 

gibbosus, Lecithaster, 80, 95 

gladius, Xyphias, 104 

Gonocerca, 77, 102 

Gonocerca phycidis, 80, 101 

grisei, Fasciola squali, 43 

griseus, Notidanus, 43 

groenlandicus, Myxocephalus, 82 

gunnellus, Pholis, 9, 81 


Halipegus ovocaudatus, 46, 56 
Haplometra cylindracea, 49 
harengus, Clupea, 8, 94 
hassalli, Hassallius, 63, 116 
Hassallius, 57 
Hassallius hassalli, 63, 116 
Hemipera, 92, 102 
Hemiuridae, 79, 90, 101 
Hemiurinae, 79, 91 
Hemiurus, 79 
Hemiurus appendiculatus, 93 
bothryophorus, 95 
communis, 93 
levinseni, 79, 92 
lithei, 93 
rugosus, 93 
hepatica, Fasciola, 29, 34 
heteroclitus, Fundulus, 9, 86 
Hippoglossus hippoglossus, 9, 88, 100, 103 
hippoglossus, Hippoglossus, 9, 88, 100, 103 
Hirudinella, 79 
Hirudinella clavata, 55, 59, 91, 104 
fusca, 59, 80, 104 
hispida, Deropristis, 110 
hispidum, Distomum, 29 
Homalometron, 79 
Homalometron pallidum, 79, 86 
Hucho perryi, 74 


inflata, Deropristis, 80, 110 
ingens, Distomum, 104 
insigne, Distomum, 43, 59, 104 


japonicum, Schistosoma, 30, 48 


Laemargus melanostoma, 43 
laevis, Raia, 14, 43 
laguncula, Aponurus, 98 
lanceolatum, Distomum, 45 
lapillus, Thais, 52 
laticauda, Genolinea, 80, 100 
Lecithaster, 79, 96 
Lecithaster confusus, 96 
gibbosus, 80, 95 
Lecithasterinae, 80 
Lecithostaphyllum, 96 


263] SOME NORTH AMERICAN FISH TREMATODES—MANTER 


Lecithostaphylinae, 79, 88 
Lecithostaphylus, 88 
Lecithophyllum, 96 
Lecithophyllum botryophoron, 98 
Lepidapedon, 79 
Lepidapedon elongatum, 79, 85 
garrardi, 84 
rachion, 79, 84 
Lepidophyllum, 88 
Lepocreadiinae, 79 
Lepocreadium, 86 
Lepocreadium album, 86 
levinseni, 86 
pegorchis, 86 
trulla, 86 
Lepodora elongata, 85 
garrardi, 84 
rachiaca, 84 
Leuceruthrus, 19, 49, 54 
Leuceruthrus microptert, 57 
levinseni, Hemiurus, 79, 92 
Lepocreadiusm, 86 
Limanda ferruginea, 9 
limanda, Pleuronectes, 94 
lintea, Raia, 14, 43 
Liocerca, 102 
littorea, Littorina, 52, 116 
Littorina littorea, 52, 116 
lobianchoi, Acanthocotyle, 111 
longa, Azygia, 63, 72, 78, 116 
longum, Distomum, 63, 66, 72, 116 
Megadistomum, 63, 116 
Joossti, Azygia, 60, 74, 116 
Lophius piscatorius, 53 
Lota maculosa, 61 
lucti, Asygia, 45, 51, 63, 68, 73, 116 
Lucioperca sandra, 77 
Lucioperca sp., 72 
luctus, Esox, 63, 72 
Lucius lucius, 61, 66 
lucius, Lucius, 61, 66 
lithei, Hemiurus, 93 
lupus, Anarrhichas, 9, 81, 103 
Lymnaeus palustris, 50 
stagnalis, 50 


macrorhyncha, Raia, 14, 53 
maculosa, Lota, 61 
masquinongy, Esox, 65, 72 
Megadistomum longum, 63, 116 
megastomum, Distomum, 55 
megastomus, Ptychogonimus, 50, 55 
melanocystis, X enodistomum, 53 
Melanogrammus aeglifinus, 9, 84 
melanostoma, Laemargus, 43 
melanostomus, Gadus, 113 
microcephalum, Distomum, 43 
microcephalus, Pleuronectes, 52 
Microgadus tomcod, 82 
Micropharynx parasitica, 9 
micropteri, Leuceruthrus, 57 
Micropterus dolomieu, 72 
salmoides, 61 
milberti, Carcharias, 43 
Mimodistomum angusticaudum, 60, 116 


minor, Dactylocotyle, 80, 112 

minor, Oclobothrium palmatum S., 112 

mollissimum, A poblema, 91, 95 
Distomum, 95 

Monogenea, 79 

monstrosa, Chimaera, 43 

Monostomum vinaledwardsit, 107 

mordax, Osmerus, 8, 72, 94 

morrhua, Gadus, 93 

Mugil capito, 92 

Myxocephalus groenlandicus, 82 


octodecims binasus, 9, 95, 103 


namaycush, Saloclinus, 72 
Neoechinorhynchus cylindratus, 10 
nicaeensis, Scymnus, 43 
Notidanus cinereus, 43 

griseus, 43 


Octobothrium minus, 112 

palmatum S. minor, 112 
Octocotylidae, 79 
Octocotylinae, 79 


octodecimspinosus, Myxocephalus, 9, 95, 103 


Ocyurus chyurus, 107 

olssoni, Podocotyle, 79, 82 

Opsanus tau, 107 

Osmerus eperlanus, 94 
mordax, 8, 72, 94 

Otiotrema, 102 

Otodistomum, 21, 54, 59, 79 


13 


Otodistomum cestoides, 10, 14, 29, 41, 44, 50, 75, 115 


veliporum, 14, 41, 55, 104, 115 


ovocaudatum, Distomum, 46 
ovocaudatus, Halipegus, 46, 56 
Oxyostoma typica, 9 


pallidum, Homalometron, 79, 86 
pelmatum, Dactylocotyle, 113 
palmatum S. minor, Octobothrium, 112 
palustris, Limnaeus, 50 
parasitica, Micropkarynx, 9 
pegorchis, Lepocreadium, 86 
Perca flavescens, 72 
perryi, Hucho, 74 
Azygia, 60, 74 
Pholis gunnellus, 9, 81 
phycidis, Dactylocotyle, 113 
Gonocerca, 80, 101 
piscatorius, Lophius, 53 
plenus, Derogenes, 103 
Pleuronectes cynoglossus, 53 
limanda, 94 
microcephalus, 52 
Podocotyle, 80 
Podocotyle atomon, 79, 81 
olssoni, 79, 82 
reflexa, 81 
Pollachius virens, 9, 94 
pompilius, Centrolophus, 43 
Proctophantastes, 88 
Prostomata, 79 
Pseudopieuronectes americanus, 3 
psora, Aega, 9 
Ptychogonimus, 54, 57 


138 ILLINOIS BIOLOGICAL MONOGRAPHS 


Ptychozonimus megastomus, 50, 55 
volgensis, 77 


rachiaea, Lepodora, 84 
rachion, Lepidapedon, 79, 84 
Distomum, 84 
radiala, Raia, 14, 43 
batis, 14, 43 
binoculata, 14, 43, 115 
clavata, 14, 43 
diaphanes, 8 
erinacea, 8, 110 
fullonica, 14, 43 
laevis, 14, 43 
lintea, 14, 43 
macrorhyncha, 14, 53 
radiata, 14; 43 
scabrata, 8 
stabuliforis, 8, 14, 43, 115 
reflexa, Podocotyle, 81 
reticulatus, Esox, 66 
Rhynchobothrius erinaceus, 10 
robusta, Asygia, 64, 73, 77 
rondeletti, Carcharias, 43 
rosaceum, Distomum, 45 
rugosus, Hemiurus, 93 


salar, Salmo, 94 
Salmo salar, 94 
sebago, 72 
trutla, 94 
salmoides, Micropterus, 61 
Salvelinus namaycush, 72 
sandra, Lucioperca, 77 
scabrata, Raia, 8 
Schistosoma japonicum, 30, 48 
scorpius, Cottus, 93 
Scomber, scombrus, 8 
scombrus, Scomber, & 
Scyllium canicula, 43 
scymni, Distomum, 43 
Scymnus nicaeensis, 43 
sebago, Azygia, 30, 63, 77, 116 
Salmo, 72 
stemerst, Distomum, 104 
simplex, Distomum, 80, 83 
Sinistroporus, 80 
Sinistroporus simplex, 80 
Siphodera, 79 
Siphoderidae, 79 
Siphodera vinaledwerdsit, 79, 107 
sphaerolecithus, Aponurus, 80, 98 
spinosus, Echinorhinus, 43 
squali grisei, Fasciola, 43 
stabuliforis, Raia, 8, 14, 43, 115 


stagnalis, Lymnaeus, 50 
Stizostedion vitreum, 61 
Steganoderma, 79, 88 
Steganoderma formosum, 79, 88 
Stephanochasminae, 79 
Stephanochasmus, 79 
Stephanochasmus baccatus, 79, 83 
Sterrhurinae, 79, 91 
Steringophorinae, 88 
Syncoeliinae, 79, 91 
Syncoelium, 102 


tau, Opsanus, 107 

Tautogolabrus adspersus, 8 
tenuis, Urophycis, 9, 82, 96, 103 
tereticolle, Azygia, 58, 63, 69, 116 


Distomum, 50, 58, 63, 69, 116 


Thais lapillus, 52 
Thunnus thynnus, 104 
thynnus, Thunnus, 104 
tobianus, Ammodytes, 94 
tomcod, Microgadus, 82 
Tristomidae, 79 

trulla, Lepocreadium, 86 
trutta, Salmo, 94 

typica, Oxyostoma, 9 


undatum, Buccinum, 52 
Urophycis chuss, 9, 92 
tenuis, 9, 82, 96, 103 


varicus, Derogenes, 80, 103 
variegatum, Distomum, 49 
veliporum, Distomum, 14, 43, 55 


Olodistomum, 14, 41, 55, 104, 115 


ventricosa, Fasciola, 55 
verrilli, Acanthocotyle, 80, 110 
verrucosum, Distomum, 55, 104 
Monostomum, 107 
vinaledwardsti, Siphodera, 79, 107 
virens, Pollachius, 9, 94 
vitreum, Stizostedion, 61 
volgense, Distomum, 77 
volgensis, Azygia, 77 
Ptychogonimus, 77 
vulgaris, Acanthias, 2 


Xenodistomum melanocystis, 53 
Xyphias gladius, 104 


Zoarces anguillaris, 9 
Zoogonidae, 79, 88 
Zoogonoides, 79, 88 
Zoogonus, 88 
Zoonogenus 88 


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